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==Part I The Early Development To The End Of The Third Day==
==Part I The Early Development To The End Of The Third Day==
==CHAPTER VIII  THE NERVOUS SYSTEM==
I. The Neuroblasts
The account given in Chapters V and VI outlines the origin
of the larger divisions of the central nervous system and ganglia.
The subsequent growth and differentiation is due to multiplication of cells, aggregation of embryonic nerve-cells, or neuroblasts, in particular regions or centers, the formation and growth
of nerve-fibers which combine to form nerves and tracts, and
the origin and differentiation of nerve-sheaths, and the supporting cells, neuroglia, of the central system. The most important
factors are the origin of the neuroblasts and of nerve-fibers in
connection with them; these fibers form the various nerve-tracts
and commissures within the central nervous system and the
system of peripheral nerves. The origin of neuroblasts and the
development of fibers is the clue to differentiation in all parts
of the nervous system.
Neuroblasts are found in two primary locations in the embryo;
(1) in the neural tube, and (2) in the series of ganglia derived
from the neural crest; these are known as medullary and ganglionic neuroblasts respectively.^
The Medullary Neuroblasts. In the neural tube of the chick,
up to about the third day, there are present only two kinds of
ceils, the epithelial cells and the germinal cells (Fig. 138).
The epithelial cells constitute the main bulk of the walls,
and extend from the central canal to the exterior; their inner
ends unite to form an internal limiting membrane lining the
central canal, and their outer ends to form an external limiting
membrane. Each cell in the lateral walls of the tube is much
elongated and usually shows three enlargements, viz., at each
end and in the region of the nucleus, the cell being somewhat
constricted between the nucleus and each end. In different
1 Neuroblasts arise also in the olfactory epithelium. (See Chap. IX.)
233
234
THE DEVELOPMENT OF THE CHICK
cells the nuclei are at different levels; thus in a section several
layers of nuclei appear. These cells are not closely packed
together, except at their outer ends, but are more or less separated
by intercellular spaces that form a communicating system of
narrow channels.
Jm.&K
277. V
Ira.'m
Fig. 138. — Section of the neural tube, 29 s embryo.
c. C, Central canal, ep. C, Epithelial cells, g. C, Germinal cells. 1. m. ex., External limiting membrane. 1. m. in.,
Internal limiting membrane. Ms'ch., Mesenchyme, m. v.,
Marginal velum.
The germinal cells are rounded cells situated next the central
canal between the inner ends of the epithelial cells; karyokinetic
figures are very common in them. According to His the germinal
cells are the parent cells of the neuroblasts alone; it is probable,
however, that they are not so limited in function, and that they
represent primitive cells from which proceed other epithelial
cells and embryonic neuroglia cells as well as neuroblasts.
THE NERVOUS SYSTEM
235
A narrow non-nucleated margin^ known as the marginal
velum, appears in the lateral walls of the neural tube external
to the nuclei (Fig, 138). This is occupied by the outer ends of
the epithelial cells. At this time, therefore, three zones may
be distinctly recognized in the walls of the neural tube, viz.,
(1) the zone of the germinal cells, including also the inner ends
of the epithelial cells, (2) the zone of the nuclei of the epithelial
cells, (3) the marginal velum. No chstinctly nervous elements
are yet differentiated.
Such elements, however, soon begin to appear: Fig. 139 represents a section through the
cord of a chick embryo of
about the end of the third day;
it is from a Golgi preparation
in which the distinctly nervous
elements are stained black, and
the epithelial and germinal
cells are seen only very indistinctly. The stained elements
are the neuroblasts, and it will
be observed that they form a
layer roughly intermediate in
position between the marginal
velum and the nuclei of the
epithelial cells. They are
usually regarded as derived
from germinal cells that have
migrated from their central
position outwards; but it is
m/Jr~,
MMf
mi.4.
Fig. 139. — Transverse section through
the spinal cord and ganglion of a
chick about the end of the third
day; prepared by the method of
Golgi. (After Ramon y Cajal.)
C, Cones of growth. Nbl. 1, 2, 3, 4,
Neuroblasts of the lateral wall (1 and
2); of the spinal ganglion (3); of the
ventral horn (motor neuroblasts) (4).
possible that some of them may have been derived from epithelial
cells. However this may be in such an early stage, it is certain
that the neuroblasts formed later are derived from germinal cells.
It will be observed that each neuroblast consists of a cellbody and a process ending in an enlargement. The process
arises as an outgrowth of the cell-body, and forms the axis cylinder or axone of a nerve-fiber; the terminal enlargement is known
as the cone of growth, because the growth processes by which
the axone increases in length are presumably located here. It
may be stated as an invariable rule that each axone process of a
medullary neuroblast arises as an outgrowth, and grows to its
236
THE DEVELOPMENT OF THE CHICK
final termination without addition on the part of other cells.
The body of the neuroblast forms the nerve-cell, from which,
later on, secondary processes arise constituting the dendrites.
The view that each nerve-cell with its axone process and
dendrites is an original cellular individual, is known as the neurone
theory. For the central nervous system this view is generally
held, but its extension to the peripheral system is opposed by
some on the ground that the axone in peripheral nerves is formed
within chains of cells, and is thus strictly speaking not an original
product of the neuroblast, though it may be continuous with the
axis cylinder process of a neuroblast. This view is discussed
under the peripheral nervous system.
Each medullary neuroblast is primarily unipolar and the
axone is the original outgrowth.
Soon, however, secondary protoplasmic processes arise from the
body of the nerve-cell and form the
dendrites. These appear first in
motor neuroblasts of the ventrolateral portion of the embryonic
cord, whose axones enter into the
ventral roots of spinal nerves (Fig.
140). The extent and kind of development of these dendritic proFiG. 140. — Transverse section cesses of the nerve-cells varies
through the spinal cord of a extraordinarily in different regions;
chick on the fourth day of Y\g^. 139, 140, and 141 give an idea
of their rapid development in the
motor neuroblasts up to the eighth
dav.
The Ganglionic Neuroblasts, The
ganglionic neuroblasts are located,
as the name implies, in the series of
ganglia derived from the neural
It must not be supposed, however, that all of the cells
incubation; prepared by the
method of Golgi. (After Ramon y CajaL)
C. a., Anterior commissure.
D., Dendrite, d. R., Dorsal root.
Ep. Z., Ependymal zone. W.,
White matter (marginal velum).
Nbl. 4, Neuroblast of the ventral
horn (motor).
crest.
of the ganglia are neuroblasts, for the ganglia contain, in all
probability, large numbers of cells of entirely different function.
(Sheath-cells, see peripheral nervous system.) It is probable
also that the neuroblasts of the spinal ganglia and some cranial
ganglia, at least, are of two original kinds, viz., the neuroblasts of
THE NERVOUS SYSTEM
237
the dorsal root and of the sympathetic system. The first kind
only is considered here, and they are usually called the ganglionic neuroblasts s.s., because they alone remain in the spinal
ganglia. Like the medullary neuroblasts these neuroblasts form
outgrowths that become axis cylinder processes; but they differ
from the latter in that each ganglionic neuroblast forms two
outgrowths, one from each end of the spindle-shaped cells, which
are arranged with their long axes parallel to the long axis of the
ganglion (Fig. 139). Thus we may distinguish a central process
and a peripheral process from each neuroblast (Fig. 139) ; the
former corresponds to the axone and the latter to the dendrites
of the medullary neuroblast. The central axone enters the dorsal
zone of the neural tube, and the peripheral process grows out into
the surrounding mesenchyme.
Fig. 141. — Transverse section through the spinal
cord of a 9-day chick, prepared by the method
of Golgi. (After Ramon y Cajal.)
Col., Collaterals, d. R., Dorsal root. G., Gray
matter. Gn., Ganglion. Nbl. 4, Neuroblast of the
ventral horn (motor), v. R., Ventral root. W.,
White matter.
In the course of the later development the cell-body moves
to one side so that the central and peripheral branches appear
nearly continuous (Fig. 141). Farther shifting of the cell-body
produces the characteristic form of the ganglionic nerve-cell with
rounded body provided with stem from which the central and
peripheral branches pass off in opposite directions. . The central
process enters the marginal velum near its dorsal boundary and
238
THE DEVELOPMENT OF THE CHICK
there bifurcates, producing two branches, one of which grows
towards the head and the other towards the tail in the dorsal
CoJ.
Fig. 142. — Six centripetal axones of the dorsal
root, rigorously copied from a good preparation
prepared according to the method of Golgi.
From a longitudinal and tangential section of
the dorsal column of the spinal cord of an 8
day chick. (After Ramon y Cajal.)
Col., Collaterals. 1, 2, 3, 4, 5, 6, the axones
entering the cord.
column of the white matter. The ascending and descending
branches send off lateral branches, collaterals, which pass deeper
into the cord, and ramify in the gray matter of the dorsal horn.
THE NERVOUS SYSTEM 239
Fig. 142 represents six central processes of ganglionic neuroblasts
entering the cord and branching as described.
After this preliminary account of the neuroblasts we may
take up the development of the spinal cord, brain, and peripheral
nervous system.
II. The Development of the Spinal Cord
We have seen that the epithelial cells of the neural tube
stretch from the lumen of the central canal to the exterior, and
that the nuclei are arranged so as to leave the outer ends free,
thus forming the marginal velum.
In the roof and floor the epithelial cells are relatively low,
and in the lateral zones much elongated. The epithelial cells
are added to at first by transformation of some of the germinal
cells; but they do not appear to multiply by division, and as
development proceeds they become more and more wideh^ separated, the interstices being filled up by neuroblasts, embryonic
glia cells, and fiber tracts. As the wall of the neural tube grows
in thickness, the epithelial cells become more and more elongated,
seeing that both external and internal connections are retained;
and, as the growth takes place mainly external to their nuclear
layer, the latter becomes reduced, relative to the entire thickness
of the neural tube, to a comparatively narrow zone surrounding
the central canal, and is now known as the ependyma (Fig. 143).
Cilia develop on the central ends of the ependymal cells in the
central canal, and from the outer end of each a branching process
extends to the periphery anastomosing with neighboring ependymal processes so as to form a skeleton or framework enclosing
the other cellular elements and fibers of the central system.
Beginning with the third day a new layer appears between
the nuclei of the epithelial cells and the marginal velum. This
layer, known as the mantle layer, is composed of neuroblasts
and embryonic glia cells, and represents the gray matter (Figs.
140 and 144). The white matter of the cord is laid down in
the marginal velum. The sources of the cells composing the
mantle layer may be twofold, viz., from the young epithelial
cells or from the germinal cells. According to some authors
young epithelial cells may be transformed into either neuroblasts
or neuroglia cells. Thus the form of the youngest neuroblasts
in Fig. 139 indicates derivation from epithelial cells, but this
240
THE DEVELOPMENT OF THE CHICK
cannot be regarded as proved. Similarly intermediate stages
between epithelial and true glia cells are apparently shown in
Fig. 143. However, there can be but little doubt that the principal source of the neuroblasts of the mantle layer is the germinal
cells, that migrate outwards between the bodies of the epithelial
cells. The germinal cells continue in active division up to at
least the eleventh day, and their activity seems sufficient to
provide for all the cellular elements of the mantle layer, whereas
the epithelial cells apparently do not divide at all. Moreover,
mitoses are not infrequent in some cells of the mantle layer itself.
Fig. 143. — Transverse section of the cord of a
nine-day chick to show neuroglia and ependymal
cells; prepared by the method of Golgi. (After
Ramon y Cajal.)
D., Dorsal. Ep., Ependymal cells. N'gl., Neuroglia cells, v., Ventral.
The form of the gray matter in the cord in successive
stages is shown in Figs. 144, 145, and 146, representing sections
of the cord at five, eight, and twelve days. It will be seen that
the gray matter gains very rapidly in importance between the
fifth and the eighth days.
Attention should be directed to a group of neuroblasts situated at
the external margin of the white matter just above the ventral roots.
This is known as Hoffmann's nucleus; it extends the entire length of the
cord (Fig. 146, twelve days).
The white matter of the cord gains in importance at an equal
rate (Figs. 144, 145, 146). Its production is due to ascending
THE XERVOUS SYSTEM
241
and descending tracts of fibers derived from medullary and
ganglionic neuroblasts. The dorsal and ventral roots of the
spinal nerves divide it on each side into three main columns,
viz., dorsal situated above the dorsal root, lateral situated between dorsal and ventral roots, and ventral situated below the
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blV
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Fig. 144. — Transverse section through the cervical swelHng
of the spinal cord of a chick, middle of the fifth day. (After
V. Kupffer.)
bl. v., Blood vessel. C. a., Anterior commissure. C, Central canal, d., Group of axones at the levelof the dorsal root^
Ep., Ependyma. N'bl., Neuroblasts,
white matter.
V. Ventral column of
ventral roots. The dorsal column begins first as a bundle of
fibers at the entrance of the fibers of the dorsal root (Fig. 144).
Subsequently, other fibers come in this region and gradually
extend towards the dorsal middle line, displacing the ependyma
242
THE DEVELOPMENT OF THE CHICK
and gray matter (Fig. 145, eight days), but the dorsal columns
of the two sides are still separated in the median line by a broad
septum of ependymal cells. Later (Fig. 146, twelve da\^s) this
septum becomes very narrow, and the accumulation of fibers in
the dorsal columns causes the latter to project on each side of
the middle line, thus forming an actual fissure between them.
Fig. 145. — Transverse section through the spinal cord, and the eighteenth
spinal ganglion of an eight-day chick.
Centr., Centrum of vertebra, d. R., Dorsal root. Ep., Ependyma. Gn.,
Spinal Ganglion. Gn. symp., Sympathetic ganglion. Gr. M., Gray matter,
m. N., Motor nucleus. R. com., Ramus communicans. R. d., Ramus dorsalis. R. v., Ramus ventralis. Sp., Spinous process of vertebra, v. R.,
Ventral root. Wh. M., White matter.
Central Canal and Fissures of the Cord. The central canal
passes through a series of changes of form in becoming the practically circular central canal of the fully formed cord. L'p to
the sixth day it is elongated dorso-ventrally, usually narrowest
in the middle with both dorsal and ventral enlargements. About
THE NERVOUS SYSTEM
243
the seventh day the dorsal portion begins to be ol^hterated by
fusion of the ependymal cells, and is thus reduced to an ependymal septum. On the eighth day this process has involved the
upper third of the canal; the form of the canal is roughly wedgeshaped, pointed dorsally and broad ventrally (Fig. 145). The
continuation of this i^rocess leaves only the ventral division as
the permanent canal.
At the extreme hind end of the cord the central canal becomes
dilated to form a relatively large pear-shaped chamber with thin
undifferentiated walls (Fig. 148); the terminal wall is still fused
with the ectoderm at eight days, and the chamber appears to
have a maximum size at this time. At eleven days the fusion
with the ectoderm still exists, and the cavitv is smaller.
s.d
' ♦.•.'•.•-••:•.'. '.••.:•::••/.■:. ■%
'i '■ ■.
'4tJ^^
Fig. 146. — Transverse section through the
cervical swelling of the spinal cord of a
12-day chick. (After v. Kupffer.)
C, Central canal, d. H., Dorsal horn of
the gray matter. Ep., Ej^endyma. N. H.,
Nucleus of Hoffmann, s. d., Dorsal fissure,
s. v., Ventral fissure, v. H., Ventral horn
of the gray matter.
The development of the so-called dorsal and ventral fissures
is essentially different. The entire ventral longitudinal fissure
of the cord owes its origin to growth of the ventral columns of
gray and white matter which protrude below the level of the
original floor (Figs. 145 and 146), and the latter is thus left between the inner end of the fissure and the central canal. The
•dorsal longitudinal fissure on the other hand is for the most part
244 THE DEVELOPMENT OF THE CHICK
a septum produced by fusion of the walls of the intermediate
and dorsal portions of the central canal; there is, however, a true
fissure produced by protrusion of the dorsal columns of white
matter (Fig. 146). This is, however, of relatively slight extent.
The original roof of the canal is therefore found between the
dorsal septum and the fissure.
Neuroblasts, Commissures, and Fiber Tracts of the Cord. The
medullary neuroblasts may be divided into four groups: (1) The
first group, or motor neuroblasts, form the fibers of the ventral
roots of the spinal nerves. These are situated originally in the
ventro-lateral zone of the gray matter (Figs. 144, 145, 146);
they are relatively large and form a profusion of dendrites (Figs.
140, 141). As they increase in number and size they come to
form a very important component of the ventral horn of the gray
matter and contribute to its protrusion. (2) The second group
may be called the commissural neuroblasts. These are situated
originally mainly in the lateral and dorsal portions of the mantle
layer, but are scattered throughout the gray matter, and their
axis cylinders grow ventrally and cross over to the opposite side
of the cord through the floor (Figs. 139 and 140), and thus form
the anterior or white commissure of the cord. (3) The cells of the
fiber tracts are scattered throughout the gray matter, and are
characterized by the fact that their axis cylinders enter the white
matter of the same side; here they may bifurcate, furnishing
both an ascending and a descending branch, or may simply turn
in a longitudinal direction. (4) Finally there are found certain
neuroblasts with a short axis cylinder, ramifying in the gray
matter on the same side of the cord. These are found in the
dorsal horn of the gray matter and develop relatively late (about
sixteen days, Ramon y Cajal).
III. The Development of the Brain
Unfortunately the later development of the brain of birds
has not been fully studied. The following account is therefore
fragmentary. It is based mainly on a dissection and sections of
the brain of chicks of eight days' incubation.
Fig. 147 is a drawing of a dissection of the brain of an eightday embryo. The left half of the brain has been removed, and
the median wall of the right cerebral hemisphere also. The
details of the cut surfaces are drawn in from sections. Figs. 148
THE NERVOUS SYSTEM
245
and 150 show median and lateral sagittal sections of the same
stage.
The flexures of the brain at this stage are: (1) the cranial
flexure marked by the 'plica encephali ventralis on the ventral
surface, (2) the cervical flexure at the junction of myelencephalon
and cord, somewhat reduced in this stage, and (3) the pontine
flexure, a ventral projection of the floor of the myelencephalon.
c/^.Pi ^- /J
U
Com.dnt. figc.op.
^ ■ — o/A
Fig. 147. — Dissection of the brain of an 8-day chick. For description see
text. The arrows shown in the figure lie near the dorsal and ventral boundaries of the foramen of Monro.
ch. PL, Choroid plexus. Com. ant., Anterior commissure. Com. post.,
Posterior commissure. C. str.. Corpus striatum. Ep., Epiphysis. H.,
Hemisphere. Hyp., Hypophysis. L. t., Lamina terminalis. Myeh, Myelencephalon. olf., Olfactory nerve, op. N., Optic chiasma. op. L., Optic
lobe. Par., Paraphysis. Paren., Parencephalon. pi. enc. v., Phca encephali ventralis. pont. Fl., Pontine flexure. Rec. op., Recessus opticus.
S. Inf., Saccus infundibuli. Tel. med., Telencephalon medium. Th., Thalamus. T. tr., Torus transversus. Tr., Commissura trochlearis.
The lines a-a, b-b, c-c, d-d, e-e, f-f, represent the planes of section A,
B, C, D, E, and F of Fig. 151.
Telencephalon. The telencephalon is bounded posteriorly,
as noted in Chapter VI, by the line drawn from the velum transversum to the recessus opticus. The telencephalon medium has
grown but little since the fourth day, but the hemispheres
246
THE DEVELOPMENT OF THE CHICK
i.p.
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y?j.a.
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■ CA
Nem.
Lt.
fiec. op.
C/j.op.
' S./nf.
i DJ/yp.
Vas.
l^/O.
Aom
Fig. 148. — Median sagittal section of an embryo of eight days.
a. A., Aortic arch. AIL, Allantois. An., Anus. A. o. m., Omphalomesenteric artery. B. F., Bursa Fabricii. b. P., Basilar plate.
C. A., Anterior commissure, c. C, Central canal. Ch. op., Optic
chiasma. C. p., posterior Commissure. CI., Cloaca. Cr., Crop,
d. Ao., Dorsal aorta. D. Hyp., Duct of the hypophysis. Ep., Epiphysis. Fis. Eus., Fissura Eustachii. Hem., Surface of hemisphere
barely touched by section. Hyp., Hypophysis. L. t., Lamina terminalis. n. A. 8, neural arch of the eighth vertebra. Nas., Nasal
THE NERVOUS SYSTEM 247
have expanded enormously, particularly anteriorly and dorsally,
and their median surfaces are flattened against one another in
front of the lamina terminalis, which forms the anterior boundary
of the telencephalon medium (Figs. 148, 149). Posteriorly the
cerebral hemispheres extend to about the middle of the diencephalon and their lateral faces are rounded. The lateral walls
of the hemispheres have become enormously thickened to form
the corpora striata (Figs. 147 and 151 A), and the superior and
lateral walls have remained relatively thin, forming the mantle
of the cerebral hemispheres (pallium). Thus the cavity of the
lateral ventricle is greatly narrowed.
The dissection (Fig. 147) shows the corpus striatum of the
right side forming the lateral wall of the hemisphere, and extending past the aperture (foramen of Monro) between the lateral
and third ventricles tow^ards the recessus opticus, where it comes
to an end.
The olfactory part of the hemispheres is not well differentiated from the remainder in the chick embryo of eight days.
There is, however, a slight constriction on the median and ventral
face (Fig. 147) which may be interpreted as the boundary of the
olfactory lobe.
The telencephalon medium is crowded in between the hemispheres and the diencephalon; its cavity forms the anterior end
of the third ventricle, and communicates anteriorly through two
slits, the foramina of Monro, with the lateral ventricles in the
hemisphere. In Fig. 147, the upper and lower boundaries of
the foramen of Monro, are indicated by the grooves on either
side of the posterior end of the corpus striatum. A hair introduced from the third ventricle into the lateral ventricle through
the foramen of Monro in the position of the arrow in Fig. 147,
can be moved up and down over the whole width of the striatum.
The lateral walls of the telencephalon medium are formed by
the posterior ends of the corpora striata and are therefore very
thick.
The lamina terminalis passes obliquely upwards and forwards
cavity. Oes., Oesophagus, p. A., Pulmonary arch, par., Paraphysis. P. C,
Pericardial cavity. Rec. op., Recessus opticus. R., Rectum. S. Inf., Saccus
infundibuli. T., Tongue. Tel., Med. Telencephalon medium. Tr., Trachea.
V. 1, 10, 20, 30, First, tenth, twentieth and thirtieth vertebral centra, r. A..
right auricle. Vel. tr., Velum transversum. V. o. m., Omphalomesenteric
vein. V. umb., Umbilical vein.
248
THE DEVELOPMENT OF THE CHICK
from the recessus opticus to the region between the foramina of
Monro. It is very thin, excepting near its center, where it is
thickened to form the torus transversus, containing the anterior
commissure. At its dorsal summit it is continuous with the
roof of the telencephalon medium, which has formed a pouchlike evagination, the paraphysis. Just behind the paraphysis
Fig. 149. — Median sagittal section of the brain of a chick embryo of 7
days. (After v. Kupffer.)
c., Cerebellum, ca., Anterior commissure, cd., Notochord. ch.. Projection of the optic chiasma. cp., Posterior commissure, e., Epiphysis,
e'., Paraphysis. hy., Hypophysis. I., Infundibulum. It., Lamina terminalis. Lop., Optic lobe. M., Mesencephalon. Mt., Metencephalon.
opt., Chiasma of the optic nerves, p., Parencephalon. ro., Recessus
opticus, s., Saccus infundibuli. se., Synencephalon. tp., Mammillary
tubercle, tp., Tuberculum posterius. tr., Torus transversus. Tr., Decussation of the trochlear nerves. Va., Velum medullare anterius. Vi.,
Ventriculus impar telencephali. vp., Velum medullare posterius.
is the velum transversum, where the roof bends upwards sharply
into the roof of the diencephalon. The epithelial wall around
the bend is folded to form the choroid plexus of the third ventricle, which is continued forward into the lateral ventricle along
THE XERVOUS SYSTEM 249
the median wall of the hemisphere, ending anteriorly in a free
branched tip (Fig. 147, ch. PI.)
The principal changes in the telencephalon since the third
day comprise: (1) great expansion of the hemispheres and
thickening of the ventro-lateral wall to form the corpora striata;
(2) origin of the paraphysis which arises as an evagination of the
roof just in front of the velum transversum about the middle of
the fifth day; (3) formation of the choroid plexus; (4) origin of
the anterior commissure within the lamina terminalis; (5) development of the olfactory region. The general morphology of the
adult telencephalon is thus well expressed at this time.
The Diencephalon has undergone marked changes since the
third day. The roof of the parencephalic division has remained
very thin, and has expanded into a large irregular sac (Figs.
147 and 148), situated between the hinder ends of the hemispheres.
The attachment of the epiphysis has shifted back to the indentation between parencephalic and synencephalic divisions, and the
epiphysis itself has grown out into a long, narrow tube, dilated
distally, and provided with numerous hollow buds. In the roof
of the synencephalic division the posterior commissure has developed (Fig. 147). In the floor the chiasma has become a thick
bundle of fibers, and the infundibulum a deep pocket, from the
bottom of which a secondary pocket (saccus infundibuli) is growing out in contact with the posterior face of the hypophysis.
Following the posterior wall of the infundibulum in its rise, we
come to a slight elevation, the rudiment of the mammillary
tubercles; just beyond this is a transverse commissure (the inferior commissure) ; and the diencephalon ends at the tuberculum
posterius.
The hypophysis has become metamorphosed into a mass of
tubules enclosed within a mesenchymatous sheath; the stalk is
continuous with a central tubule representing the original cavity
from which the other tubules have branched out (Fig. 148), and
it may be followed to the oral epithelium from which the whole
structure originally arose. (See note at end of this chapter.)
The lateral walls of the diencephalon have become immensely
thickened, both dorsally and ventrally, and a deep fissure (Fig.
147) is found on the inner face at the anterior end, between the
dorsal and ventral thickenings. The deepest part of the fissure
is a short distance behind the velum transversum; from this a
250
THE DEVELOPMENT OF THE CHICK
'""W^: K.
tf
Bth^ \ -'^ ^ r - " ^'^^^^. Go//
/ .
f y''
.i^
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/
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Fig. 150. — Lateral sagittal section of an embryo of 8 days. Right side of
the body.
All. N., Neck of the allantois. Cbl., cerebellum. Cr., Crop. E. T., Egg
THE NERVOUS SYSTEM 251
short spur runs forward, a still shorter one ventrally, and the
longest arm extends backwards, gradually fading out beyond
the middle of the diencephalon. This fissure is not a continuation
of the sulcus Monroi, or backward prolongation of the foramen
of Monro, but is, on the contrary, entirely independent.
The lateral thickenings of the diencephalon constitute the
thalami optici, each of which may be divided into epithalamic,
mesothalamic, and hypothalamic subdivisions. In the chick at
eight days there is a deep fissure between the epi- and mesothalamic divisions (the thalamic fissure. Fig. 147). The substance
of the epithalamus forms the ganglion habenulse. The mesothalamic and hypothalamic divisions are not clearly separated.
The transition zone between the diencephalon and mesencephalon
is sometimes called the metathalamus.
The mesencephalon has undergone considerable changes since
the third day. The dorso-lateral zones have grown greatly in
extent, at the same time becoming thicker, and have evaginated
in the form of the two large optic lobes. Hence the median
portion of the roof is sunk in between the lobes (Fig. 147), and is
much thinner than the walls of the lobes. The dorso-lateral
zones and roof thus form a very distinct division of the mesencephalon, known as the tectum lohi optici. The ventro-lateral
zones and floor have thickened greatly and form the basal division of the mesencephalon. The ventricle of the mesencephalon
thus becomes converted into a canal (aqueduct of Sylvius), from
which the cavities of the optic lobes open off.
In the metencephalon likewise there is a sharp distinction
between the development of the dorso-lateral zones and roof,
on the one hand, and the ventro-lateral zones and floor on the
other. From the former the cerebellum develops in the form
of a thickening overhanging the fourth ventricle. This thickening is relatively inconsiderable in the middle line (cf. Figs. 148
and 150). Thus the future hemispheres of the cerebellum are
tooth. Eust., Eustachian tube. Gn. 1, 13, First and thirteenth spinal
granglia. Gon., Gonad. Hem., Hemisphere. Lag., Lagena. Lg., Lung. M.,
Mantle of Hemisphere. Msn., Mesonephros. Olf. L., Olfactory lobe. Olf.
N., Olfactory nerve. P. C, Pericardial cavity. Pz. 5, The fifth post-zygapophysis. R. C. 1, 2, Last two cervical ribs. R. th. 1, 5, First and fifth thoracic ribs. S. pc-per., Septum pericardiaco-peritoneale. S'r., Suprarenal.
Symp., Main trunk of the sympathetic. Str., Corpus striatum. V. 1, 10,
20, 30, First, tenth, twentieth and thirtieth vertebral arches. V. C. I., Vena
cava inferior. V. L. L., Ventral ligament of the liver.
252 THE DEVELOPMENT OF THE CHICK
indicated. The surface is still smooth at the eighth day, but
on the tenth and eleventh days folds of the external surface
begin to extend into its substance, without, however, invaginating its entire thickness. These are the beginnings of the cerebellar fissures.
The floor and ventro-lateral zones of the metencephalon enter
into the formation of the pons.
In the roof of the isthmus, or constricted region between
cerebellum and mesencephalon, is found a small commissure
produced by decussation of the fibers of the trochlearis (Fig. 147).
In the wall of the myelencephalon the neuromeres have disappeared. The thin epithelial roof has become more expanded
in the anterior part (Figs. 147 and 148). Floor and sides have
become greatly thickened.
Commissures. The brain commissures existing at eight days
are the anterior, posterior, inferior, and trochlearis (Fig. 149).
In the next four or five days two more appear, viz., the commissura pallii anterior (Kupffer), corresponding to the corpus
callosum of mammalia and the commissura habenularis.
The development of the various nuclei and fiber tracts of
the bird's brain is entirely unknown and affords an interesting
topic for research.
IV. The Peripheral Nervous System
The peripheral nervous system comprises the nerves which
span between peripheral organs and the central nervous system.
There are fifty pairs in a chick embryo of eight days, of which
twelve innervate the head, and thirty-eight the trunk, distinguished respectively as cranial and spinal nerves. It is convenient for purposes of description to consider cranial and spinal
nerves separately, and to take up the spinal nerves first because
they are much more uniform in their mode of development
than the cranial nerves, and also exhibit a more primitive or
typical condition, on the basis of which the development of the
cranial nerves must be, in part, at least, explained.
The Spinal Nerves. Ear-h spinal nerve may be divided into
a somatic portion related primarily to the somatopleure and axis of
the embryo, and a splanchnic portion related primarily to the
splanchnopleure and its derivatives. In each of these again a
motor and sensory component may be distinguished. Thus each
THE NERVOUS SYSTEM
253
y&/./f
'S.S^r.
D
- '/f.
str
l'JeJ./7]^o'.)
W^^
,op.L.
Tr ^
#
B
^//.if^-'
Fig. 1.51. — Six transverse sections through the brain of an 8-day chick in
the planes represented in Fig. 147.
Cbl., Cerebelhim. F. M., Foramen of Monro. Gn. V., Ganghon of the
trigeminus. Isth., Isthmus. It. d., Diverticuhmi of the iter. lat. V.,
Lateral ventricle. Other abbreviations as before (Fig. 147).
254 THE DEVELOPMENT OF THE CHICK
spinal nerve has four components, viz., somatic motor, somatic
sensor}^, splanchnic motor, and splanchnic sensory, the two latter
constituting the so-called sympathetic nervous system. It is
obvious, of course, that the splanchnic components must be
missing in the caudal nerves. The somatic and splanchnic components will be considered separately.
Somatic Components. Each spinal nerve arises from two roots,
dorsal and ventral (Fig. 145). The fibers of the former arise from
the bipolar neuroblasts of the spinal ganglia; the fibers of the ventral root, on the other hand, arise from a group of neuroblasts in
the ventral portion of the cord. The roots unite in the intervertebral foramen to form the spinal nerve. Typically, each spinal
nerve divides almost immediately into three branches, viz., a dorsal branch, a ventral branch, and a splanchnic branch to the sympathetic cord; the last is known as the ramus communicans.
Fig. 145 represents a section passing through the twentieth
spinal nerve of an eight-day chick. The dorsal and ventral roots
unite just beneath the spinal ganglion; fibers are seen entering
the sympathetic ganglion (ramus communicans); the ventral
branch passes laterally a short distance where it is cut off;
beyond this point it can be traced in other sections in the
next posterior intercostal space more than half-way round the
body-wall; that is, as far as the myotome has extended in its
ventral growth. The dorsal branch arises at the root of the
ventral and passes dorsally in contact with the ganglion to
branch in the dorsal musculature and epidermis. This nerve may
be regarded as typical of the spinal nerves generally.
There are thirty-eight spinal nerves in an embryo of eight
days. The first two are represented only by small ventral roots.
The first two spinal ganglia are rudimentary in the embryo and
absent in the adult, hence the ganglion illustrated in Fig. 145 is the
eighteenth of the functional series (see Fig. 149) ; it lies between the
nineteenth and twentieth vertebra?.
The fourteenth, fifteenth, and sixteenth are the principal
nerves of the brachial plexus, and have unusually large ganglia.
The twenty-third to the twenty-ninth are the nerves of the leg
plexus, the thirtieth to the thirty-second innervate the region
of the cloaca and the remainder are caudal. The special morphology of the spinal nerves does not belong in this description.
THE NERVOUS SYSTEM 255
There are one or two vestigial ganglia behind the thirty-eighth nerve,
evidently in process of disappearance at eight days.
The early history of the spinal nerves is as follows: The axis
cylinder processes of the fibers begin to grow^ out from the neuroblasts about the third day (cf. p. 235). At this time the myotomes are in almost immediate contact with the ganglia; thus
the fibers have to cross only a very short space before they enter
the myotome. The further growth is associated with the growth
and differentiation of the myotome between which and the
embryonic nerve there is a very intimate relation of such a sort
that the nerve follows the myotome and its derivatives in all
changes of position. Thus nerves do not need to grow long
distances to establish their connections, but these are formed
at a very early period. This accounts for the motor fibers; the
way in which the sensory fibers, that arise from the spinal ganglia,
reach their termination is not known.
Sheath-cells and Cell-chain Hypothesis. No embryonic nerve
consists entirely of axones, but, from the start, each nerve trunk
contains numerous nuclei. The latter belong to cells which have
been given two radically different interpretations, corresponding
to two distinct theories concerning the neuraxone.
(1) The first theory, knowm as the neurone theory, is the one
tacitly followed in the preceding description and may be stated
as follows: the nerve-cell, dendrites and axone, including the
terminal arborization, constitute a single cellular individual or
unit, differentiated from the neuroblast alone. The nuclei in
the embryonic nerves therefore belong to cells that are foreign
to the primary nerve. Their function is to form the various
sheaths of the nerves, viz., the sheaths of the individual axones
and the endo-, peri-, and epineurium. The sheath of Schwann
arises from such cells that envelop the individual fibers at suitable
distances and spread longitudinally until neighboring sheath cells
meet; each such place of meeting constitutes a node of Ranvier.
Until recently it has been universally believed that the sheath
cells arose from the mesenchvme; but recent observations on Amphibia and Selachia have shown that they arise from the ganglia
in these forms; their original source is therefore the ectoderm. It
is probable that they have the same origin in the chick, though this
has not been demonstrated by direct observation or experiment.
(2) The second theory is known as the cell-chain hypothesis.
256 THE DEVELOPMENT OF THE CHICK
According to this the axones of peripheral nerves arise as differentiations of the sheath-cells in situ; continuity of the axone is
established by arrangement of these cells in rows, and union
with the neuroblast is essentially secondary. The entire axone
is thus by no means an outgrowth of the neuroblast; at most its
proximal portion is.
Bethe (1903) expresses the idea thus: "Between the cord of
the embryo and the part to be innervated there is formed primarily
a chain of nuclei around which the protoplasm is condensed.
This is fundamentally an extended syncytium in which the nuclei
of the neuroblasts and of the nerve-primordium lie. Within
the denser protoplasm which appears as the body of the nervecells, axones differentiate by condensation, and these extend
from one cell to the next, and so on to the condensations which
are called neuroblasts. The differentiated axones tend more
and more to occupy the center of the embryonic nerve, where
they appear to lie free, though as a matter of fact they are still
embedded in the general plasma which is no longer distinctly
visible on account of its lesser density. Since the axones remain
in firm connection with the neuroblasts, it appears in later stages
as if they were processes of these and had nothing to do with
their original formative cells."
This view is essentially that of Balfour, Beard, and Dohrn;
the neurone hypothesis was first clearly formulated in embryological terms by His, and has been supported by the investigations of a considerable number of observers, notably Ramon y
Cajal, Lenhossek and Harrison.
The neurone hypothesis has far stronger embryological support than the cell-chain hypothesis; moreover, it is the only
possible hypothesis of the development of nerve tracts in the
central system, because cell-chains are entirely lacking here during the formation of these tracts. In recent years it has been
demonstrated that isolated neuroblasts in culture media produce
complete axones, sheath cells being entirely absent. Thus the
cell-chain hypothesis has received its final quietus, and is now of
historical interest only. (Burrows 1911, Lewis and Lewis 1911.)
Splanchnic Components (Sympathetic Nervous System). Two
views have been held concerning the origin of the sympathetic
nervous system: (a) that it is of mesenchymal origin, its elements
arising in situ; (b) that it is of ectodermal origin, its elements
THE NERVOUS SYSTEM 257
migrating from the cerebro-spinal ganglia to their definitive
positions. The first view was held by the earlier investigators
and was originally associated with the extinct idea that the spinal
ganglia were mesenchymal in origin; the view has been entirely
abandoned. The second view was partly established with the
discovery that the spinal ganglia are of ectodermal origin, and
that the ganglia of the main sympathetic trunk arise from the
spinal ganglia; but there is some difference of opinion yet in
regard to the peripheral ganglia of the symphathetic system,
and especially the plexuses of Meissner and Auerbach in the walls
of the intestine. However, the preponderance of evidence and
logic favors the view of the ectodermal origin of the entire sympathetic nervous system.
The first clear evidences of the sympathetic nervous system
of the chick are found at about the end of the third or the beginning of the fourth day; at each side of the dorsal surface of the
aorta there is found in cross-section a small group of cells massed
more densely than the mesenchyme and staining more deeply.
Study of a series of sections shows these to be a pair of longitudinal cords of cells beginning in the region of the vagus, where
they lie above the carotids, and extending back to the beginning
of the tail; the cords are strongest in the region of the thorax,
and slightly larger opposite each spinal ganglion. Cells similar
to those composing the cords are found along the course of the
nerves up to the spinal ganglia, and careful study of earlier stages
indicates that the cells composing the cords have migrated from
the spinal ganglia. The two cords constitute the primary sympathetic trunks.
Fig. 152 is a reconstruction of the anterior spinal and sympathetic ganglia of a chick embryo of four days. The primary
sympathetic trunk is represented by a cord of cells enlarged
opposite each ganglion and united to the spinal nerve by a cellular process, the primordium of the ramus communicans. In the
region of the head the segmental enlargements are lacking.
No other part of the sympathetic nervous system is formed
at this time with the exception of a group of cells situated in the
dorsal mesentery above the yolk-stalk; these are destined to
form the ganglion and intestinal nerves of Remak. They have
not been traced back to the spinal ganglia, but it is probable
that such is their origin.
258 THE DEVELOPMENT OF THE CHICK
In the course of the fourth and fifth days aggregations of
sympathetic gangUon cells begin to appear ventral to the aorta,
and in the mesentery near the intestine. The connection of these
with the primary cord is usually rendered evident by agreement
in structure, and by the presence of intervening strands of cells;
moreover, in point of time they always succeed the primary cord,
so that their origin from it can hardly be doubted.
About the sixth day the secondary or permanent sympathetic
trunk begins to appear as a series of groups of neuroblasts situated just median to the ventral roots of the spinal nerves. They
r~
Fig. 152. — Reconstruction in the sagittal plane
of the anterior spinal and sympathetic ganglia of a chick embryo of 4 days. (After
Neumayer.)
Ceph. S., Cephalic continuation of the sympathetic trunk. S. C, Sympathetic cord. Sg.,
Sympathetic ganghon. sp., Spinal nerve, spg.,
Spinal ganglion. R. C, Ramus communicans.
are thus separated from the spinal ganglia only by the fibers
of the ventral roots between which neuroblasts may be found,
caught apparently in migration from the spinal to the sympathetic ganglion. The number of these secondary sympathetic
ganglia is originally 30, one opposite the main vagus ganglion,
and each spinal ganglion to the twenty-ninth (Fig. 150). Soon
after their origin they acquire three connections by means of
axones, viz., (a) central, with the corresponding spinal nerve
THE NERVOUS SYSTEM 259
root by means of strong bundles of fibers; (b) peripheral, with
certain parts of the original primary sympathetic cord; (c) longitudinal, the entire series being joined together by two longitudinal
bundles of fibers uniting them in a chain. The central connections constitute the rami communicantes , and are as numerous as
the sympathetic ganglia themselves; but so close is the approximation of the sympathetic ganglion to the roots of the spinal
nerves that they are not visible externally, the ganglion appearing to be sessile on the root (Fig. 145); sections, however, show
the fibers. The peripheral connections constitute the various
nerves of the abdominal viscera; these are not metameric;
their number and arrangement is shown in Figure 153.
In the period between the fourth and the eighth da}^ the primary sympathetic cord becomes resolved into the various ganglia
and nerves constituting the aortic plexus, the splanchnic plexus,
and the various ganglia and nerves of the wall of the intestine.
Remak's ganglion has grown and formed connections with the
splanchnic plexus, and other parts of the primary sympathetic
cord. The details of these various processes are too complex
for full description; they are included in part in Figs. 153 and 154.
Ganglia and Nerves of the Heart. The development of the
cardiac nerves is of special interest on account of its bearing on the
physiological problem of the origin of the heart-beat. The heart
of the chick begins to beat long before any nervous connections
with the central system can have been established; indeed, the
rhythmical pulsation begins at about the stage of 10 somites
when the neural crest is yet undifferentiated, and no neuroblasts
are to be found anywhere. Either, then, the heart-beat is of muscular origin (myogenic), or, if of nervous origin, the nerve-cells
concerned must exist in the wall of the cardiac tube ah initio.
The first trace of nerve-cells is found in the heart of the chick
about the sixth day. These cells are at the distal ends of branches
of the vagus, with which they have grown into the heart. Previous to this time these neuroblasts are found nearer to the vagus
along the course of the arteries. There can be but little doubt
that they have arisen from the vagus ganglion and that they
reach the heart by migration. Such an origin has been demonstrated with great probability for all the known nervous elements
of the heart of the chick. (See Wilhelm His, Jr., Die Entwickelung
des Herznervensystems bei Wirbelthieren.)
260
THE DEVELOPMENT OF THE CHICK
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THE NERVOUS SYSTEM
261
If any cardiac nervous elements arise in situ, they certainly
remain undifferentiated until those that have a ganglionic origin
have already entered the heart.
The Cranial Nerves. Tlie nerves of the head exhibit a much
greater degree of heteronomy than the spinal nerves, and, in
spite of much study, knowledge of their embryonic development
is still in a very unsatisfactory condition. The same principles,
however, apply to the development of both cranial and spinal
nerves; the axones of the former like those of the latter arise
either from medullary or ganglionic neuroblasts which are respectively unipolar and bipolar; but the cranial ganglionic and
Fig. 154. — Diagram of the relations of the
parts of the sympathetic nervous system
as seen in the cross-section. (After His,
Jr.)
M., mesentery. Msn., Mesonephros.
Other abbreviations same as Fig. 153.
medullary nerve-nuclei are not similarly segmented, as in the
case of the spinal nerves, and hence the axones are not related
as dorsal and ventral roots of single nerve trunks; nor has the
attempt to interpret the cranial nerves as homologues of dorsal
and ventral roots respectively been successful in the case of the
most important nerves. Moreover, the olfactory and optic nerves
differ from the spinal type even more fundamentally. The olfactory is a sensory nerve that arises apparently from the olfactory
262 THE DEVELOPMENT OF THE CHICK
epithelium, and the optic is really comparable to an intramedullary nerve tract, seeing that its termination lies in a part of the
original wall of the neural tube, viz., the retina.
Groups of medullary neuroblasts giving rise to axones of
motor cranial nerves are located in the brain as follows, according
to His:
Oculo-motor nucleus in the mid-brain.
Trochlearis nucleus in the isthmus.
Motor trigeminus nucleus in the zone of the cerebellum, including
the descending root.
Abducens and facialis nuclei, beyond zone of greatest width
of the fourth ventricle (auditory sac zone).
Glossopharyngeus, vagus, in the region of the calamus scrip
torius.
Accessorius and hypoglossus, in the region extending to the
cervical flexure.
These constitute the cranial motor nerve nuclei, and are more
or less discontinuous.
The ganglionic nerves or nerve-components of the head arise
from the following primitive embryonic ganglion-complexes:
1. Complex of the trigeminus ganglia.
2. Complex of the acustico-facialis ganglia.
3. Complex of the glossopharyngeus ganglia.
4. Complex of the vagus ganglia.
The early history of these ganglion-complexes has already been
considered; they are called complexes because each forms more
than one definitive ganglion. It is probable also that each contains sympathetic neuroblasts, which may separate out later as distinct ganglia, thus reseml)ling the spinal sympathetic neuroblasts.
There is no close agreement in the segmentation of the motor
neuroblasts within the brain and that of the ganglion complexes.
For instance, in the region of the trigeminal ganglionic complex,
the motor nuclei of the oculo-motor, trochlearis, and trigeminus
are found, and in the region of the vagus ganglionic complex,
the motor nuclei of vagus, accessorius, and hypoglossus. Thus
the medullary and ganglionic nerves of the head are primitively
separate by virtue of their separate origins. They may remain
entirelv so, as in the case of the olfactory, trochlearis, and abducens, or they may unite in the most varied manners to form
mixed nerves.
THE NERVOUS SYSTEM 263
The motor nuclei of the oculo-motor, trochlearis, abducens,
and hypoglossus nerves He in the same plane as the motor nuclei
of the spinal nerves, i.e., in the line of prolongation of the ventral
horns of the gray matter. The motor nuclei of the trigeminus,
facialis, glossopharyngeus, vagus, and spinal accessory on the
other hand lie at a more dorsal level, and the roots emerge therefore above the level of origin of the others. It will be noted that
these are the nerves of the visceral arches, whereas those cranial
nerves that continue the series of spinal ventral roots innervate
myotomic muscles, like the latter. Similarly the ganglia of the
pharyngeal nerves (V, VII, IX, and X) differ from spinal ganglia
in certain important respects: the latter are derived entirely
from the neural crest, whereas a certain portion of each of the
primary cranial ganglia is derived from the lateral ectoderm of
the head, as noted in the preceding chapter. Thus the pharyngeal nerves form embryologically a class by themselves, both
as regards the medullary and also the ganglionic components.
1. The Olfactory Nerve. The embr3'onic origin of the olfactory
nerve has been a subject of much difference of opinion: thus it
has been maintained by a considerable number of w^orkers that
it arises from a group of cells on each side situated between the
fore-brain and olfactory pits; some of these maintained that
these cells arose as an outgrowth from the fore-brain, others
that they came from the epithelium of the olfactory pit, and
yet others that this group of cells, or olfactory ganglion, was
derived from both sources. This group of cells was supposed
by some to include a large number of bipolar neuroblasts, one
process of which grew towards the olfactory epithelium and
the other towards the fore-brain, entering the olfactory lobe
and ending there in terminal arborization. This view is, however,
in conflict with the ascertained fact that the fibers of the fully
formed olfactory nerve are centripetal processes of olfactory
sensory cells situated in the olfactory epithelium.
The most satisfactory account of the origin of the olfactory
nerve in the chick is that of Disse. This author finds two kinds
of cells in the olfactory epithelium of a three-day chick, viz.,
epithelial cells, and germinal cells which become embryonic
nerve-cells or neuroblasts. At this time the olfactory epithelium
is separated from the w^all of the fore-brain by only a very thin
layer of mesenchyme. Early on the fourth day axones arise
264
THE DEVELOPMENT OF THE CHICK
from the central ends of the neuroblasts and grow into the
mesenchyme towards the fore-brain. At the same time groups
of epithelial cells free themselves from the inner face of the
olfactory epithelium, and come to lie between this and the forebrain. The axones of the neuroblasts grow between these cells
until they reach the base of the fore-brain over which they spread
out, entering the olfactory lobe about the sixth day (Figs. 155
and 156). In the meantime the peripheral ends of the olfactory
neuroblasts have extended out as broad protoplasmic processes
to the surface of the olfactory epithelium, and thus form the percipient part of the olfactory sense-cells.
Fig. 155. — Olfactory epithelium of a chick embryo of 5
days, prepared by the method of Golgi. (After Disse.)
a, b, and c indicate different forms of neuroblasts in the
olfactory epithelium.
The epithelial cells between fore-brain and olfactory pit, through
which the axones of the olfactory neuroblasts grow, are for the
most part supporting and sheath-cells of the nerve, but they include a few bipolar neuroblasts (Fig. 156). The latter are to
be considered as olfactory neuroblasts with elongated protoplasmic processes.
Rubaschkin finds a ganglion, which he calls ganglion olfactorium
nervi trigemini, situated beneath the olfactory epithelium in a nineday chick. The bipolar cells send out processes peripherally which end
in fine branches between the cells of the olfactory mucous membrane,
and centrally, which go by way of the ramus olfactorius nervi
trigemini towards the Gasserian ganglion.
2. The Second Cranial or Optic Nerve. The course of this
THE NERVOUS SYSTEM
265
nerve is entirely intramedullary, the retina being part of the
wall of the embryonic brain; its development will therefore be
considered in connection with the development of the eye.
Fig. 156. — Sagittal section through the head of a chick embryo of 5 days,
showing the floor of fore-brain, olfactory pit, and developing olfactory
nerve between. (After Disse.)
a., Unipolar neuroblasts near the olfactory epithelium, b., Bipolar cell
in the olfactory nerve, c, Unipolar cell near the brain. F. B., Floor of
fore-brain. N'bl., Neuroblast in the olfactory epithelium, olf. Ep., Olfactory epithelium, olf. N., Olfactory nerve, olf. P., Cavity of olfactory pit.
3. The third cranial or oculo-motor nerve arises from a group
of neuroblasts in the ventral zone of the mid-brain near the median
line, and appears external to the wall of the brain at about sixty
hours (about 28-30 somites). At this time it appears as a small
group of axones emerging from the region of the plica encephali
266 THE DEVELOPMENT OF THE CHICK
ventralis, and ending in the mesenchyme a short distance from
its point of origin. At seventy-two hours the root is much
stronger, interpenetrated with mesenchyme and ends between
the optic cup and floor of the brain behind the optic stalk (cf.
Fig. 101). At ninety-six hours the root is broad and fan-shaped,
the nerve itself is comparatively slender, and passes downwards
and backwards behind the optic-stalk where it enters a welldefined ganglion situated just median to the ophthalmic branch
of the trigeminus; this is the ciliary ganglion; beyond it the
fibers of the oculo-motor turn forward again to enter the region
of the future orbit.
According to Carpenter (1906) the ciliary ganglion arises
from two sources: (a) migrant medullary neuroblasts that pass
out into the root of the oculo-motor, and follow its course to
the definitive situation of the ciliary ganglion, and (b) a much
smaller group of neuroblasts that migrate from the ganglion of
the trigeminus along the ophthalmic branch, and by way of a
ramus communicans to the ciliary ganglion. The adult ciliary
ganglion show\s correspondingly two component parts: (a) a
larger ventral region composed of large bipolar ganglion cells,
and (6) a smaller dorsal region containing small ganglion cells
with many sympathetic characters. It is probable that the
medullary fibers of the oculo-motor nerve are distributed entirely
to the muscles innervated by it, viz., the superior, inferior, and
internal rectus and inferior oblique muscles of the eye. The
fibers arising from the neuroblasts of the ciliary ganglion terminate peripherally in the intrinsic muscles of the eye-ball, and
centrally (in the case of the bipolar cells) in the brain, which
they reach by way of the medullary nerve. The motor branches
leave the trunk of the nerve a short distance centrally to the
ciliary ganglion.
4. The trochlearis or fourth cranial nerve is peculiar inasmuch as it arises from the dorsal surface of the brain in the
region of the isthmus. It arises entirely from medullary neuroblasts and innervates the superior oblique muscle of the eye.
Marshall states that it may be readily seen in a five-day embryo;
in an embryo of eight davs it is a slender nerve arising from the
dorsal surface of the isthmus immediately in front of the cerebellum ; the fibers of the two sides form a commissure in the roof
of the isthmus (Fig. 148).
THE NERVOUS SYSTEM 267
5. The trigeminus or fifth cranial nerve consists of motor
and sensory portions. The latter arises from the trigeminal
ganglion, the origin of which has already been described. The
ganglionic rudiment appears roughly Y-shaped even at an early
stage (cf. Figs. 105 and 117), the short stem lying against the
wall of the brain and the two branches diverging one in the direction of the upper surface of the optic cup (ophthalmic branch)
and the other towards the mandibular arch. The original connection of the ganglion with the roof of the neural tube is lost
during the second day and permanent connection is established
during the third day, presumably by growth of axones into the
wall of the brain. The new connection or sensory root of the
trigeminus is attached to the myelencephalon in the region of
greatest width of the fourth ventricle near the ventral portion
of the lateral zone.
During the fourth day the peripheral axones follow the direction of the ophthalmic and mandibular branches of the ganglion
and grow out farther as the ophthalmic and mandibular nerves;
the former passes forward between the optic vesicle and the wall
of the brain; the latter runs ventrally towards the angle of the
mouth, over which it divides, a smaller maxillary branch entering
the maxillary process of the mandibular arch, and a larger one,
the mandibular nerve, runs into the mandibular arch. (For an
account of the branchial sense organ of the trigeminus, see Chap.
VI.)
A medullary component of the trigeminal nerve arises from
the wall of the brain just median to the ganglionic root during
the fourth day; it runs forward parallel to the ganglionic ophthalmic branch, and sends a twig to the ciliary ganglion. Beyond
this point it unites with the ganglionic branch.
A connection of the trigeminus with the olfactory sensory
epithelium is described under the olfactory nerve.
6. The sixth cranial or abducens nerve is stated to arise about
the end of the fourth day. It is a purely motor nerve, and has
no ganglion connected with it; it innervates the external rectus
muscle of the eye. At 122 hours it arises by a number of slender
roots attached to the myelencephalon near the mid- ventral line,
beneath the seventh nerve. Its roots unite into a slender trunk
that runs directly forward beneath the base of the brain to the
region of the orbit. The sixth nerve thus corresponds more
268 THE DEVELOPMENT OF THE CHICK
nearly than any other cranial nerve to a ventral spinal nerveroot.
7 and 8. The Facial and Auditory Nerves. The ganglia of
these nerves at first form a common mass, the acustico-facialis.
But during the course of the fourth day the anterior and ventral
portion becomes distinctly separated from the remainder and
forms the geniculate ganglion; the remainder then forming the
auditory ganglia (cf. Fig. 102). The acustico-facialis ganglion
complex moves from its original attachment to the dorsal surface
of the brain and acquires a permanent root during the third day,
attached ventrally just in front of the auditory sac.
(a) The seventh cranial or facialis nerve arises during the
fourth day from the geniculate ganglion which is situated just
above the second or hyomandibular branchial cleft. It grows
first into the hyoid arch (posttrematic branch), but towards
the end of the fourth day a small branch arises just above the
cleft and arches over in front of it and runs down the posterior
face of the mandibular arch (pretrematic branch). The origin of
the motor components is not known.
(h) The further history of the auditory nerve is considered
with the development of the ear.
9. The ganglion of the ninth cranial or glossopharyngeal nerve
(ganglion petrosum cf. Fig. 102) arises from the anterior part of
the postotic cranial neural crest as already described. Early on
the fourth day the ganglionic axones enter the base of the brain
just behind the auditory sac and establish the root, which consists of four or five parts on each side. From the ganglion which
is situated at the summit of the third visceral arch a strong
peripheral branch develops on the fourth day, and extends into
the same arch; a smaller anterior branch develops a little later
which passes over the second visceral pouch and enters the
second visceral arch. About the same time an anastomosis is
formed with the ganglion of the vagus.
10. The tenth cranial or vagus (pneumogastric) nerve is very
large and complex. Its ganglion very early shows two divisions,
one near the roots (ganglion jugulare) and the other above the
fourth and fifth visceral arches (ganglion nodosum cf. Fig. 102).
It arises by a large number ot fine rootlets on each side of the
hind-brain behind the glossopharyngeus, and the roots converge in
a fan-like manner into the proximal ganglion; from here a stout
THE NERVOUS SYSTEM 269
nerve passes ventrally and enters the ganglion nodosum situated
above the fourth and fifth visceral arches. Branches pass from
here into the fourth and fifth arches, and the main stem is continued backward as the pneumogastric nerve s.s. From the hinder
portion of the spreading roots a strong commissure is continued
backward parallel to and near the base of the neural tube as far
as the fifth somite; this is provided with three small ganglion-like
swellings. This condition is found about the end of the fourth
day. Later this commissure unites with the main sympathetic
trunk, and part of the vagus ganglion separates from the remainder as the ganglion cervicale primum of the sympathetic trunk.
During the fifth and sixth days the main stem of the vagus
grows farther back and innervates the heart, lungs, and stomach.
Neuroblasts of the sympathetic system accompany the vagus
in its growth, and form the various ganglion cells of the heart,
and other organs innervated by the vagus.
During the fifth and sixth days the ganglion nodosum, which
originally lay at the hind end of the pharynx, is carried down
with the retreat of the heart into the thorax, and on the eighth
day it is situated at the base of the neck in close contact with
the thymus gland.
11. The Eleventh Cranial or Spinal Accessory Nerve. No observations on the development of this nerve in the chick are
known to me.
12. The twelfth cranial or hypoglossus nerve appears on the
fourth day as two pairs of ventral roots opposite the third and
fourth mesoblastic somites; each root is formed, like the ventral
roots of the spinal nerves, of several bundles that unite in a common slender trunk; ganglia are lacking, as in the first and second
cervical nerves. The roots of the hypoglossus are a direct continuation of the series of ventral spinal roots, and as they are
related to somitic muscle plates in the same way as the latter,
there can be no doubt of their serial homology with ventral roots
of spinal nerves. The first four mesoblastic somites are subsequently incorporated in the occipital region of the skull, and
thus the hypoglossus nerve becomes a cranial nerve. No nerves
are formed in connection with the first and second mesoblastic
somites. As the occipital region of the skull forms in the region
of the occipital somites, two foramina are left on each side for
exit of the roots of the hypoglossus (Figs. 150 and 244).
270 THE DEVELOPMENT OF THE CHICK
During the fourth and fifth days the nerve grows back above
the roof of the pharynx, then turns ventrally behind the last
visceral pouch and forward in the floor of the pharynx.
According to Chiarugi minute ganglia are formed in the second,
third, and fourth somites: but they soon degenerate (fourth day) without
forming nerves.
Note: The structure called "hypophysis" on p. 249, sometimes called
Rathke's pouch, forms only the anterior lobe or glandular part of the hypophysis of adult anatomy; the posterior lobe of the hypophysis is derived
from the structure called " saccus infundibuli " in this chapter, which is a derivation of the floor of the brain.


==CHAPTER IX  ORGANS OF SPECIAL SENSE==
==CHAPTER IX  ORGANS OF SPECIAL SENSE==

Revision as of 16:19, 21 July 2019

THE DEVELOPMENT OF THE CHICK - AN INTRODUCTION TO EMBRYOLOGY BY

FRANK R. LILLIE

PROFESSOR IN THE UNIVERSITY OP CHICAGO

SECOND EDITION, REVISED

NEW YORK HENRY HOLT AND COMPANY

1919

Copyright, 1908, 1919,

BY

HENRY HOLT AND COMPANY


Part I The Early Development To The End Of The Third Day

CHAPTER IX ORGANS OF SPECIAL SENSE

I. The Eye

The development of the eye up to the stage of 36 somites has been already described. We shall now consider the subsequent changes in the following order: (1) optic cup, (2) vitreous body, (3) lens, (4) anterior chamber, cornea, iris, etc., (5) choroid and sclerotic, (6) the conjunctival sac and eyelids, (7) the choroid fissure and the optic nerve.

1. The optic cup at the stage of 36 somites is composed of two layers, an inner, thicker layer, known as the retinal layer, and an outer, thinner layer, known as the pigment layer; these are continuous with one another at the pupil and choroid fissure. The inner and outer layers come into contact first in the region of the fundus, and the cavity of the original optic vesicle is gradually obliterated. The choroid fissure is in the ventral face of the optic cup; it is very narrow at this time, and opens distally into the pupil; centrally it ends at the junction of optic stalk and cup, not being continued on the stalk as it is in mammals (Fig. 157).

The walls of the optic cup may be divided into a lenticular zone {pars lenticularis or pars cceca) and a retinal zone; the former includes the zone adjacent to the pupil, not sharply demarcated at first from the remainder or retinal zone, but later bounded distinctly by the ora serrata. The retinal zone alone becomes the sensitive portion of the eye; the lenticular zone develops into the epithelium of the iris and ciliary processes.

In the lenticular zone the inner and outer layers become actually fused, but in the retinal zone they may always be separated; indeed, in most preparations they are separated by an actual space produced by unequal shrinkage.

The differentiation of the lenticular from the retinal zone begins about the seventh day, when a marked difference in thick 271


272


THE DEVELOPMENT OF THE CHICK


ness appears. The transition from the thinner lenticular to the thicker retinal zone soon becomes rather sudden in the region of the future ora serrata. About the eighth or ninth day a further differentiation arises within the lenticular zone, marking off the regions of the iris and ciliary processes (Fig. 159). The region



ep ^es p r


157 ■ 158

Fig. 157. — Section through the eye of a chick embryo at the

beginning; of the fourth day of incubation. (After Froriep.)

ch. Fis. I., Lip of the choroid fissure. Di., Lateral wall of the diencephalon. V, \", Distal and proximal walls of the lens, st., Optic stalk.

Fig. 158. — Section of the distal portion of the eye of a chick,

second half of the fifth day of incubation. (After Froriep.)

c. ep. int., Internal epithelium of the cornea. Corn, pr., Cornea propria. Ect., Ectoderm, ep.. Epidermis. ir.,Iris. mes.. Mesoderm, p., Pigment layer of the optic cup. r., Retinal layer of the optic cup.

of the iris is a narrow zone bounding the pupil in which the two la3'ers of the optic cup become blended so that pigment from the outer layer invades the inner layer; the epithelia are decidedly


ORGANS OF SPECIAL SENSE


273


u.e. /.


C/2.

cj7.


irjs


ant. (•/?. Corri.


ITj^



^ — op.n .


■olf.


/i .m


Fig. 159. — Frontal section of the eye of an eight day chick. Shrinking in the process of preparation has caused a separation between the retinal and pigment layers, ant. ch., Anterior chamber of the eye. ch., Choroid coat, cil., Ciliary processes. Corn., Cornea. 1. e. 1., Lower eyelid, n. m., Nictitating membrane, olf., Olfactory sac. op. n., Optic nerve, o. s., Ora serrata. p., Pigment layer of the optic cup. post, ch., Posterior chamber of the eye. ret.. Retina, scl., Sclerotic coat. scl. C, Sclerotic cartilage, u. e. 1., Upper eyelid.

thinner than in the ciliary region. The mesenchyme overlying the iris early becomes condensed to form the stroma of the iris; the epithelia form the uvea of the developed iris (Fig. 159). The muscles of the iris (sphincter pupillse) are stated by


274


THE DEVELOPMENT OF THE CHICK


Nussbaum, Szily, and Lewis to arise from epithelial buds of the pupillary margin and the adjacent portion of the pigment layer of the iris. The marginal buds (Fig. 160) begin to form during the seventh day, the more peripheral ones somewhat later; the former are less numerous and larger than the latter. The observations are well supported, and appear to leave no doubt that the specificity of the ectoderm cells of the iris is not fixed. According to Lewis the wandering pigmented cells of the anterior portion, at least, of the choroid also arise from the pigment layer of the optic cup.

The ciliary processes begin to form from the ciliary region of the lenticular zone on the eighth day (Fig. 159) ; the epithelium

^M" Sph. Sfih. ^-"


ES.


3pM



B.


Fig. 160. — Two sections of the pupillary margin of the eye of a chick of 13 days' incubation. A., X 260. B., 130. (After Lewis.) c. P., Ciliary process. E. B., Epithelial bud. P., Margin of pupil, p. 1., Pigment layer of Iris. r. 1., Retinal layer of iris. Sph., Bud for the formation of the sphincter muscle of the iris, derived from the margin. Sph.', Sph.", Submarginal buds of the sphincter.

becomes thrown into folds projecting towards the posterior chamber, the cavity of the folds being filled by the mesenchyme of the developing choroid coat. The muscles of the ciliary body develop from the mesenchyme of the processes, which acquire a connection with the lens through a special differentiation of the vitreous body, the zonula ciliaris (zonula Zinnii).

In the retinal portion of the optic cup the inner la3^er forms the entire retina proper from the internal limiting membrane to the rods and cones inclusive. The outer layer forms the pig


ORGANS OF SPECIAL SENSE 275

ment layer of the retina. About the middle of the fourth day pigment begins to develop in the outer layer and extends throughout it, even to the distal portion of the optic-stalk at first (Ucke, '91). The histogenesis of the retina of the chick has been described by Weysse (1906).

2. The Vitreous Humor (Corpus Vitreum). Until comparatively recently embryologists have adhered to the view stated by Schoeler (1848) and Kolliker (1861) that the vitreous body arises from mesenchymal cells that enter the e3^eball through the choroid fissure. The fact that the embryonic vitreous humor of birds is almost entirely devoid of cells was a serious difficulty. The cells are in fact so scanty as to be absent in many entire sections. Moreover, in character they resemble embryonic blood-cells and not mesenchyme, and disappear entirely by the eighth day. It seems impossible that they should play any important part in the origin of the massive vitreous body. Researches of the last few years have demonstrated that the vitreous body is primarily of ectodermal origin, its fibers arising as processes of cells of the inner layer of the optic cup and the matrix as secretion. According to some the cells of the lens are responsible wholly (Lenhossek) or in part (S/ili) for the fibers; this view, however, has been strongly combatted (Kolliker and Rabl) and requires further evidence to substantiate it.

Both retinal and csecal parts of the cup take part in the formation of the fibers of the vitreous body; the retinal part is at first the most important, and the primary vitreous body is almost entirely retinal in its origin. But after the caecal part is differentiated the activity of the retinal part becomes less, and the greater part of the fillers of the vitreous body appears to be formed from cells of the csecal part, that send out branching and anastomosing processes into the posterior chamber. There is no sharp boundary between the fibers that form the vitreous body and those that form the zonula; and the fibers of the latter may be regarded as homologous to those of the former. The matrix of the embryonic vitreous body may be regarded as a secretion of the walls of the optic cup. Later, the secretion appears to be confined to the ciliary processes. It is possible that the mesenchyme plays some part in the formation of the vitreous body after the formation of the pecten begins; but there is no evidence that it does so at first.


276 THE DEVELOPMENT OF THE CHICK

3. The Lens. The account of the development of the lens is mainly after Rabl. The wall of the lens-sac is everywhere a single-layered epithelium, though the nuclei are at different levels in

the cells.

Shortly after the lens-sac has become separated from the ectoderm the proximal wall (that next the cavity of the optic cup) begins to thicken by elongation of the constituent epithelial cells (Figs. 157 and 158). During the fourth day the elongation of the cells increases greatly as the first step in the formation of the lens fibers, while those of the distal wall remain practically unchanged, being destined to form the epithelium of the lens. Between the cells of the proximal and distal walls are found ceUs of an intermediate character, bounding the equator of the lens (Fig. 158).

During the fifth day the elongation of the cells of the proximal waU proceeds apace; those in the center of the wall are most elongated and there is a gradual decrease towards the equator of the lens. In this way the face of the proximal wall gradually approaches the distal wall and meets it on the fifth day, thus obliterating the central part of the lens ca\ity, though the peripheral part remains open for a considerably longer time (Fig. 158). The nuclei of the lens fibers occupy approximately their center, and thus form a fairly broad curved band, concave towards the optic cup. At the same time the lens is increasing very rapidly

in size.

During the sixth, seventh, and eighth days the same processes continue and the elongation of the lens fibers makes itself felt on the inner face of the lens which becomes convex. The form and arrangement of the parts is shown in Figure 159. The fibers already present are destined to form only the core of the adult lens; and a new process begins at this time, leading to the formation of fibers that wrap themselves around this core in a meridional direction and form many concentric layers (666 according to Rabl). These new concentric fibers proceed from cells situated between the core fibers and the lens epithelium, that is, around the equator of the lens. There is a very rapid multiplication of cells here; those next the core transform into fibers arranged meridionally on the surface of the core; others develop over these and thus the original fibers come to be surrounded by more and more concentric layers. At first these are disposed rather irregularly, but soon the arrangement becomes extraordinarily regular.


ORGANS OF SPECIAL SENSE


277


This process is kept up not only during embryonic life, but during the entire growth of the fowl; thus the thickness of the superimposed lamellae is only 0.60 mm. at hatching, but is 2.345 mm. in the adult (Rabl).

In the fowl the lens includes three concentric layers of fibers: (1) the central mass or core formed by the proximal wall of the original lens-sac; this has the same diameter (0.80 mm.) as the entire fiber mass at eight days. Nuclei are entirely absent. (2) An intermediate layer of meridional rows of fibers rather irregularly arranged, which shade gradually into the fibers of the core and into those of (3) the radial lamellae, which form the greater part of the substance of the adult lens. The meridional rows and the radial lamellae proceed from the cells of the intermediate zone of the original lens-sac. Fig. 161 shows a sector of an equatorial section through the lens of a chick. The three zones are well marked; the extraordinary regularity of the superimposed layers of the radial lamellae is well shown.

The lens epithelium of birds and reptiles also produces a peculiar structure which may be called the equatorial ring (Ringwulst, Rabl).

It will be seen in the figures




^


f&^ #'


Fig. 161. — Equatorial section through the lens of a chick embryo of eight days. The main mass of the entire lens is represented by irregularly arranged central fibers. Towards the surface (above) the fibers are arranged in rows and are quite regularly six sided. (After Rabl.)


278 THE DEVELOPMENT OF THE CHICK

that the epithelium is originally thinnest distally and thickens towards the equator. This condition increases up to the eighth day, at which time the thickening increases more a short distance from the equator, so that there is a broad ring-shaped thickening of the anterior epithelium separated by a narrow thinner zone from the cells of the equatorial zone (cf. Fig. 159). This ring increases in thickness during the greater part of the period of incubation, and its cells become fibers arranged in a radial direction. The meaning of this curious structure is somewhat obscure, but from the fact that it shows on its surface the impression of the ciliary processes, Rabl w^as of the opinion that it served in accommodation of the eye as an intermediary between the ciliary processes and the true lens-fibers.

4. Anterior Chamber and Cornea, etc. When the optic vesicle is first formed it is in immediate contact with the ectoderm. After its invagination the lips of the optic cup withdraw a short distance from the surface. At the same time the lens invaginates and is cut off from the ectoderm, but rem.ains in contact with it during the third day. There is thus a ring-shaped space between the lens and optic cup on the one hand and the ectoderm on the other, which is the beginning of the anterior chamber of the eye (cf. Fig. 96 C). With the formation of the cornea the lens withdraws somewhat from the surface and the space spreads over the whole external surface of the lens; at first it is very narrow, but increases in size by the formation of the iris and the bulging of the cornea.

The cornea itself develops from two sources: (1) the external epithelium is derived from the ectoderm overlying the anterior chamber, (2) the cornea propria and the internal epithelium lining the anterior chamber develop from the surrounding mesenchyme but in somewhat different ways.

The cornea propria appears on the fourth day as a delicate structureless membrane beneath the corneal epithelium. During the fifth day it increases to about the thickness of the overlying ectoderm (Fig. 158). About this time mesenchyme cells from the margin of the optic cup begin to migrate between the cornea propria and lens, and soon form a single complete layer of cells on the inner face of the cornea propria; this layer becomes the inner epithelium of the cornea (Fig. 158). The cornea propria is still devoid of cells, but on the sixth and


ORGANS OF SPECIAL SENSE 279

seventh days the mesenchyme surroimding the eyeball begins to penetrate it from all sides in the form of a compact wedge, which, advancing in the substance of the cornea propria, soon meets in the center. These cells form the so-called corpuscles of the cornea. They appear arranged in strata from a very early period.

The anterior chamber is bounded by the cornea externally; its margins, which are at first coincident with the lips of the optic cup, soon extend peripherally over the iris (Fig. 159). The inner epithelium ceases at the margin of the cavity or is continuous with the cells of the sclerotic; it does not appear, in an eight-day chick at any rate, to be reflected over the iris, but the epithelium of this structure next the anterior chamber appears to be simply a special differentiation of its own superficial cells. The anterior chamber is closed centrally by the lens, but communicates more or less for a considerable period around its margin with the posterior chamber. This is at least the appearance in good sections; it seems probable, though, that in life there is contact between the optic cup and lens.

The stroma of the iris proceeds from that portion of the mesenchyme left in association with the pars iridis retinae after the peripheral extension of the anterior chamber. It becomes very vascular at an early stage. The canal of Schlemm arises as a series of vacuoles just peripheral to the margin of the anterior chamber about the eighth day. These soon run together to form a ring, which is separated from the anterior chamber by the ligamentum pectinatum iridis.

5. The choroid and sclerotic coats are differentiations of the mesenchyme surrounding the optic cup. But little is known concerning the details of their development in the chick. A figure of Kessler's shows chromatophores developed in the choroid coat at twelve days; I find a very few already formed at eight days. Cartilage begins to appear in the sclerotic at eight days, the forerunner of the sclerotic ossicles (Fig. 159).

6. The Eyelids and Conjunctival Sac. The integument over the embrvonic eveball remains unmodified until about the seventh day. At this time a circular fold of the integument forms around the eyeball with the pupil as its center. At the same time a semi-lunar fold develops within the first on the side of the eyeball next the beak. (See Figs. 122-124.) From the


280 THE DEVELOPMENT OF THE CHICK

first fold the upper and lower eyelids are developed, and from the second the third eyelid or nictitating membrane. The area bounded by the outer ring-shaped fold becomes the conjunctival sac.

From their place of origin the free edges of these folds then grow towards the center, and thus a cavity, the conjunctival sac, is formed between the folds and the integument over the eyeball (conjunctiva sclerse). The outer fold grows more rapidly above and below than at the sides and the opening narrows, becoming, therefore, gradually elhptical and finally somewhat spindle-shaped. Thus the upper and lower eyelids are established. The semi-lunar fold of the embryonic nictitating membrane also grows towards the pupil, most rapidly in its center. The conjunctival sac also expands peripherally, especially at the inner angle of the eye, and thus accommodates itself to the increasing size of the eyeball (Fig. 159).

The Harderian gland is visible on the eighth day as a solid ingrowth of ectodermal cells of the conjunctival sac at the innermost angle of the nictitating membrane.

Feather germs develop on the outer surface of both upper and lower lids especially at their edges. The ectoderm covering the inner faces of the upper and lower lids, both faces of the nictitating membrane and the remainder of the conjunctival sac becomes modified into a moist mucous membrane. Over the cornea the ectoderm is especially modified as already noted.

Papillce Conjunctiva Sclerce. On the seventh day of incubation papillae begin to appear on the surface of the conjunctiva sclerse and soon form a ring surrounding the iris at some distance peripheral to its margin (Figs. 122, 123 and 124). The number of these papillae appears to be quite constantly fourteen. They are at first fully exposed owing to the undeveloped condition of the eyelids, but the latter overgrow them about the eleventh or twelfth days. Degeneration of the papillae begins about this time, and on the thirteenth day they have entirely disappeared. In section they are found to be thickenings of the ectoderm, produced by multiplication of the cells. They may rise above the surface; but more frequently project inwards towards the connective tissue. There is apparently no accompanying hypertrophy of the latter. Thus they differ quite essentially from feather germs with which it seems natural to compare them; and their significance is entirely problematical (see Xussbaum).


ORGANS OF SPECIAL SENSE 281

7. Choroid Fissure, Pecten, and Optic Nerve. The pecten of the hen's eye is a pigmented vascular plate inserted in the depression occupying the center of the elongated blind spot, or entrance of the optic nerve, which extends meridionally from the fundus nearly to the ora serrata. The pecten projects a considerable distance into the posterior chamber and its free edge is much longer than its base, being consequently folded like a fan; hence the name. The optic nerve runs along the base of the pecten, its fibers passing off on either side into the retina; thus it continually diminishes in size until it disappears. The pecten is consequently separated from the choroid coat by the optic nerve. It is supposed to function as a nutrient organ for the layers of the retina, by means of lymph channels that pass off from its base into the retina. There is no arteria centralis retinae in the

bird's eye.

These structures develop in connection with the choroid fissure as follows: On the fourth day the choroid fissure has become a very narrow slit, and by the middle of the day its edges are in apposition in the pars cceca of the bulbus. Proximally, however, the meeting of the lips of the fissure is prevented by the mesoblast, in which the basal blood-vessel runs along the entire length of the open portion of the fissure. During the fourth day this blood-vessel enters the posterior chamber Avith its enveloping mesenchyme along the entire length of the open portion of the choroid fissure, and forms a low mesenchymal ridge connected by a narrow neck of mesenchyme in the fissure with the mesenchyme outside. During the fifth day the ridge becomes higher and keel-shaped, and a thickening appears along part of its free edge above the blood-vessel. During this day also fusion of the lips of the choroid fissure has taken place in the pars caeca. At the same time an important change begins in the proximal portion of the choroid fissure that leads to the formation of the pecten proper. This is an involution of the lips of the optic cup bounding the choroid fissure on each side of the mesodermal keel, and their continuous ingrowth until they meet over the keel and fuse above it in a mass in which the outer and inner layers of the retina are indistinguishably fused. Thus the proximal portion of the mesodermal keel is enclosed in a kind of tunnel composed of the involuted edges of the optic cup. The formation of this tunnel progresses gradually from the fundus towards


282


THE DEVELOPMENT OF THE CHICK


the ora serrata by the same process of involution, until on the eighth day the mesodermal keel is completely covered up.

Fig. 162 gives a diagrammatic view of the condition of the pecten in the middle of the seventh day of incubation. Figs. 163 and 164 show sections through this at the points a, h, c, d, e, indicated in the figure. The formation of the tunnel will be readily understood by study of the figures. It will be seen that the major portion of the embryonic pecten is of ectodermal origin, and that the mesoderm forms a relatively inconspicuous part of it. Later, on the same day, it becomes increasingly difficult


CAfi^^


P.




i PB.


H^



Fig. 162. — Diagrammatic reconstruction of the pecten of the eye of a chick embryo of 1\ days' incubation. (After Bernd.)

Ch. fis. 1., Lip of the choroid fissure. Ch. fiss., Choroid fissure. Mes., Mesoblast. Mes. b., Boundary of the mesoblast within the choroid fissure. Mes. K., Thickening of the mesoblastic keel. op. C, Optic cup. O. St., Optic stalk. P., Pecten. P. B., Base of the pecten.

The arrow indicates the direction of growth of the ectodermal tunnel.

The lines a, b, c, d, e show the planes of the sections reproduced in Fig. 163 (a, b, c, e) and in Fig. 164 (d).

to distinguish ectodermal and mesodermal portions of the pecten, and thereafter it is quite impossible to say which parts of it are of ectodermal and which are of mesodermal origin. During the eighth and ninth days the pecten increases greatly in height, and becomes relatively very much narrower.

The folds of the pecten now begin to develop and, b}^ the seventeenth day their number is 17-18, the same as in the adult. The pigment does not begin to appear until about the twelfth day. The details of the development of the blood-vessels are not known.


ORGANS OF SPECIAL SENSE


283


The Optic Nerve. Owing to the relations established by the choroid fissure, the floor of the optic stalk is continuous from the first with the inner layer of the retina (Fig. 96 B), and it furnishes the path along which the optic nerve grows. The axones of the optic nerve originate, for the most part, from the retinal neuroblasts, composing the layer next to the cavity of the optic cup, and their growth is thus centripetal. They are first formed in the fundus part of the retina, and grow in the direction of the



Mes ft




Fig. 163. — Outlines of sections in the planes a, b, c, e, of

Fig. 163. (After Bernd.)

bl. v., Blood vessel, i. 1., Inner or retinal layer of the optic cup. o. 1., Outer or pigment layer of the optic cup. P. inv., Angle of invagination of the pecten. Other abbreviations as before. (Fig. 162.)


optic stalk between the internal limiting membrane and the neuroblast layer (ganglion cell layer), thus forming a superficial layer of axones; their formation begins on the fourth day, and there is a period about the end of this day when axones are found in the distal part of the optic stalk, next to the bulbus oculi, but not in the proximal part, next to the brain. This observation affords conclusive proof of the retinal origin of the fibers of the optic


284


THE DEVELOPMENT OF THE CHICK


nerve; moreover, at an early stage of their differentiation it is possible to trace their connection with retinal neuroblasts.

The first fibers of the optic nerve are formed, as already stated, from the fundus part of the retina; the fibers, therefore, pass directly to the floor of the optic stalk; but on the fifth day the formation of fibers begins from more distal portions of the retina and these do not grow towards the insertion of the optic stalk, l3ut towards the choroid fissure; arrived there, they bend centrally and run in a bundle on each side along the floor of the bulbus oculi to the optic stalk, where they join with the fibers first formed. The later formed fibers pass to still more distal portions



■ Mes/I


P.,






t-«*f;


«^:Mfe^2^




Fig. 164. — Section in the plane of d of Fig. 162, to show the histological structure. (After Bernd.) Abbreviations as before.


of the choroid fissure, and, as the pecten forms in the manner already described, the fibers of the optic nerve all unite beneath it on their way to the original optic stalk. Thus, the optic nerve obtains an insertion coincident in length with the base of the pecten, and its fibers, radiating off into the retina on each side of the pecten, separate the latter completely from the choroid coat of the eyeball.

The optic stalk is at first a tubular communication between the optic vesicle and the fore-brain, and its walls are an epithelial layer of the same thickness throughout. The fibers of the optic


ORGANS OF SPECIAL SENSE 285

nerve grow into its ventral wall exclusively, between its epithelial cells, which gradually become disarranged and irregular. Thus the ventral wall becomes increasingly thick and the lumen excentric. By the sixth day the lumen appears in cross-section as a narrow lenticular space with an epithelial roof, above the large optic nerve. Soon after, the lumen disappears entirely; no trace of its former existence is to be found on the eighth day.

II. The Development of the Olfactory Organ

The origin of the olfactory pit, external and internal nares, and olfactory nerve, has already been considered (pp. 169, 215, and 263). Before the formation of the internal and external nares, not only has the entire olfactory epithelium become invaginated, but, owing to the elevation of internal and external nasal processes, the pit has become so deepened that the margin of the olfactory epithelium proper now lies a considerable distance within the cavity. That part of the nasal cavity thus lined with indifferent epithelium is known as the olfactory vestibule. After the fusion of the internal nasal process with the external nasal and maxillary processes, the cavity deepens still more.

The choanse lie at first just within the oral cavity, but the palatine processes of the maxillary process, growing inwards across the primitive oral cavity (pp. 298, 299), unite on the sixth or seventh day at their anterior ends with the internal nasal processes, and thus cut off an upper division of the primitive oral cavity at its anterior end from the remainder; in this way the internal openings of the nasal cavities into the oral cavity are carried back of the primitive choanae; they are henceforward known as the secondary choanse. Further growth of the palatine processes brings them nearly together in the middle line along the remainder of their length, about the eleventh day; but fusion does not take place, the birds possessing a split palate. Thus the superior division of the primitive oral cavity is added to the respiratory part of the nasal passages.

The nasal cavity is further elaborated between the fourth and eighth days by ingrowths from the lateral wall (turljinals) and by the formation of the supraorbital sinus as an evagination that grows outwards above the orbit. Three turbinals are formed in the nasal cavities, viz., the superior, middle, and inferior turbinals. These arise as folds of the lateral wall projecting into


286 THE DEVELOPMENT OF THE CHICK

the lumen, the superior and middle from the olfactory division proper, and the inferior from the vestibulum; on the middle turbinal, however, the sensory epithelium gradually flattens out to the indifferent type. The middle turbinal appears first in the ventral part of the olfactory division, about the beginning of the fifth day, and the superior somewhat later, immediately above the former, the two being separated by a deep groove (Fig. 165). The vestibular turbinal arises still later, and is well formed on the eighth day.

Fig. 166 shows a reconstruction of the nasal cavity, seen from the lateral side, of an embryo of about seven days. It is a reconstruction of the epithelium, and thus practically a mold of the cavity; therefore projections into the cavity appear as depressions in the model, and the grooves and outgrowths of the external wall as projections. The superior turbinal has an oval shape with the long axis in an apical direction; it is bounded by a fairly deep depression, the elevated margin of the model, from the lower end of which the supra-orbital sinus (S. s'o.) passes off ventrally and externally. The deep depression immediately below the superior turbinal lodges the median turbinal. A fairly long passage leads off from its neighborhood to the choanse and a shorter one, the vestibulum, to the external nares. The depression in the wall of the vestibulum is caused by the vestibular or inferior turbinal. The palatine and maxillary sinuses are not yet formed.

The external nares are closed during the greater part of the period of incubation by apposition of their walls. The form and dimensions of the nasal cavities change greatly during incubation, owing to shifting in the original positions of the turbinals, outgrowth of the facial region, and development of sinuses. The details are not very well investigated, and an examination of them would lead too far.

There has been a good deal of discussion as to the existence of an organ of Jacobson in the nose of birds; it has usually been assumed that it is entirely absent even in the embryo. Others have identified the ducts of nasal glands as a modification of this organ. Recently, however, Cohn has described a slight evagination in the median wall of the primary olfactory pit, that agrees precisely in its form and relationship with the first rudiment of the organ of Jacobson in reptiles. Although it persists only from the stage of about 5.3 mm. to about the stage of


ORGANS OF SPECIAL SENSE


287


5.9 mm. head-length, he identifies it positively as a rudimentary organ of Jacobson.

The septal gland arises on the eighth day from the inner wall of the vestibulum, opposite the base of the vestibular tur


FiG. 165. — Transverse section of the olfactory organ of a chick embryo, of 7.5 mm. head length. (After Cohn.) f., Line of fusion, e. n., External nasal process, i. n., Internal nasal process. T. 1, T. 2, Intermediate and superior turbinals.

binal, as a solid cord of cells. This grows backwards in the nasal septum and passes to the outer side and branches, subsequentlyj acquiring a lumen.


288


THE DEVELOPMENT OF THE CHICK


III. The Developmext of the Ear

The ear develops from two entirely different primary sources, viz., the otocyst,and the first visceral or hyomandibular cleft : The former furnishes the epithelium of the membranous lab^-rinth; the entodermal pouch of the latter becomes the tympano-eustachian cavity; and part of the external furrow forms the external auditory meatus; the tissue between the internal pouch and the external furrow develops into the tympanum. The mesenchyme in the neighborhood of each of these primordia becomes modified,




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Ch., Choanal, e. N., External nares. S. s'o., Supraorbital sinus. T. 1, T. 2, T. 3, Intermediate, superior and inferior (vestibular) turbinals.

(1) to form the bony labyrinth, perilymph, and other mesenchymal parts of the internal ear, and (2) to form the auditory ossicles of the middle ear. Thus the ear furnishes a striking example of the combination of originally diverse components in the formation of a single organ. The course of evolution of this complex senseorgan is thus illustrated in the embryonic development; in the Selachia the hyomandibular cleft is a communication between pharynx and exterior, like the branchial clefts, and still preserves to a certain extent the respiratory function. The embryonic history furnishes a summary of the way in which it was gradually


ORGANS OF SPECIAL SENSE


289



drawn into the service of the otocyst in the course of evohition.

Development of the Otocyst and Associated Parts. In Chapter VI we took up the formation of the otocyst and the origin of the endolymphatic duct. The Letter is at first an apical outgrowth from the otocyst, but its attachment soon becomes shifted to the median side of the otocyst, owing to the expansion of the dorsal external wall of the latter (Fig. 167). Three divisions of the otocyst may now be distinguished: (a) ductus endolymphaticus or recessus labyrinthi; (6) pars superior labyrinthi; (c) pars inferior labvrinthi. The boundarv between the two latter is rather indistinctly indicated at this stage by a shallow groove on the median face of the otocyst. The development of these parts may now be followed separately.

(a) The Development of the Ductus Endolymphaticus. It was noted in Chapter VI that the ductus endolymphaticus is united to the epidermis by a strand of cells that preserves a lumen up to the stage of 104 hours at least (Fig. 98). Shortly after, this connection is entirely lost.

The opening of the endolymphatic duct into the otocyst appears to be shifted more and more ventrally along the median surface, with the progress of differentiation of the other parts of the otocyst, until it lies in the region of communication of the utriculus, sacculus and lagena (Figs. 168 and 171). This is brought about by the various foldings and expansions of the wall of the otocyst described in b and c. In the meantime the endolymphatic duct has increased in length with the growth of the surrounding parts, and on the sixth day the distal half begins to expand to form the saccus endolymphaticus, lying between the utriculus and the hind-brain. The elongation of the entire endolymphatic duct and the enlargement of the saccus continue during the seventh day, and on the eighth day the saccus overtops


Fig. 167. — Model of the otocyst of a chick embryo shortly before its separation from the ectoderm. (After Krause.)

D. e., Endolymphatic duct. Ect., Ectoderm, p. v., Pocket for formation of vertical semicircular canals. X indicates the strand of cells uniting the endolymphatic duct to the ectoderm.


290


THE DEVELOPMENT OF THE CHICK


the hind-brain and bends in above it towards the middle line (Fig. 168). The right and left sacci are, however, still separated by a considerable space. The walls of the saccus already form a large number of low folds, presumably glandular, the first begin


FiG. 168. — Transverse section through the head of a chick embryo of eight

days in the region of the ear (photograph).

C. a., Anterior semicircular canal. C. h., Horizontal semicircular canal. Caps, and., Auditory capsule. Cav. Tymp., Tympanic cavity. Col., Columella. Duct end., Endolymphatic duct. ex. au. M., External auditory meatus. Fis. Tub., Tubal fissure. Lag., Lagena. M. C, Meckel's cartilage. Myel., Myelencephalon. N'ch., Notochord. p'l.. Perilymph. Sac, Sacculus. Sac. end.. Endolymphatic sac. Tub. Eust., Eustachian tube. Tymp., Tympanum. L^tr., Utriculus. X., Sac derived from the inner extremity of the tympanic cavity.


nings of which were visible on the sixth day. The form of the saccus and ductus endolymphaticus at a somewhat later stage is shown in the reconstruction (Fig. 173).


ORGANS OF SPECIAL SENSE


291



It is interesting to note that the epidermic attachment to the endolymphatic duct is about at the junction of the saccus endolymphaticus and ductus endolymphaticus s.s. If this may bear a phylogenetic interpretation, it would seem that the saccus should be regarded as an addition to the primitive ductus of Selachii, which opens on the surface.

(b) Development of the Pars Superior Lahyrintki; Origin of the Se7nicircular Canals. We have already seen that the shifting of the ductus endolymphaticus to the median surface of the otocyst is brought about by a vertical extension of the superior lateral wall of the otocyst, w'hich forms a shallow pocket opening widely into the otocyst (Fig. 167). Slightly later a second pocket is formed by a horizontally extended evagination of the lateral w^all of the pars superior directed towards the epidermis. These two pockets, known as the vertical and horizontal pockets, are the forerunners of the semicircular canals : the vertical of both anterior and posterior, and the horizontal of the horizontal semicircular canal. The horizontal pocket forms at about the middle of the external surface on the fifth day; immediately above it is a roughly triangular, pear-shaped depression in the wall of the otocyst, bounded by the vertical pocket on the other tw^o sides. Thus the vertical pocket consists of two divisions, anterior and posterior, meeting at the apex of the otocyst (Fig. 169) « 

The pockets gradually deepen; and the semicircular canals arise from them by the fusion of the walls of the central part of each pocket, thus occluding the lumen except at the periphery (Fig. 170). The fused areas subsequently break through. The peripheries thus form semicircular tubes communicating at each end with the remainder of the superior portion of the otocyst, or ntriculus, as it may now be called. Three semicircular canals are thus formed, one from each division of the original vertical pocket and one from the horizontal pocket. The upper ends of the anterior and posterior semicircular canals, formed from the anterior and posterior divisions of the vertical pocket, open together into


Fig. 169. — Model of the auditory labyrinth (otocyst) of a chick embryo of undetermined age ; view from behind. (After Rothig and Brugsch.)

C. 1., Pocket for the formation of the lateral (horizontal) semicircular canal.

C. v., pocket for formation of vertical semicircular canals.

D. C, PrimonHum of ductus cochlearis and lagena. D. e., endolymphatic duct.


292


THE DEVELOPMENT OF THE CHICK



the apex of the utricukis; and the horizontal canal formed from the external pocket extends between the separated lower ends of the other two.

We must now proceed to a more detailed examination. In

point of time the anterior (sagittal) semicircular canal is the first to be formed (Fig. 171) ; the external (horizontal or lateral) canal comes next, and considerably later the posterior (frontal). Thus the anterior canal is at first the largest, the external next, and the posterior the smallest. These differences are, however, largely compensated in the course of the embryonic development. The ampullae appear as dilations in the pockets even before the canals are Pig. 170. — Model of the auditory formed, and are conspicuous dilalabyrinth of a chick embryo of 6 tions by the time that the central days and 17 hours; external view, parts of the pockets have broken (After Rothig and Brugsch.) throuo'h (Fig. 172).

C. a., Pocket for formation of „. ^^^ ^^„ , ,, _^^u^+^

anterior semicircular canal. C.I., FlgS. 1/0-1/3 show the pocketS

Pocket for formation of lateral ^Tid canals at six days seventeen semicircular canal. C. p., Pocket , , _+^^„ u^tt,.^

for formation of posteriir semicir- hours, seven days seventeen houis,

cular canal. D. c, Ductus coch- eight days seventeen hours, and

learis. D. e., Endolymphatic duct. . ^ , ■> ,^ j La., LagenL eleven days seventeen hours. It

will be seen that, whereas the anterior and lateral canals are formed from the start in planes at right angles to one another, viz., the sagittal and horizontal, the posterior canal is not at first in the third or transverse plane, but gradually assumes it.

The form of the utriculus is gradually assumed during the formation of the semicircular canals; it becomes drawn out into a roughly triradiate form, so that it consists of a central cavity and three sinuses, viz., the median sinus which receives the end of the anterior and posterior semicircular canals, the posterior sinus situated above the ampulla of the external semicircular canal, and the anterior sinus in the region of the ampullae of the horizontal and sagittal semicircular canals (cf. Fig. 173). A short distance in front of the posterior sinus on the median face of


ORGANS OF SPECIAL SENSE


293


the utriculus occur the openings of the ductus endolymphaticus, sacculus, and ductus cochlearis; the two latter derived from the pars inferior of the otocyst, to the development of which we now turn.

(c) Development of the Pars Inferior Lahyrinthi; Lagena, Ductus Cochlearis, and Sacculus. During the changes described in the pars superior labyrinthi, the pars inferior has developed into the ductus cochlearis and lagena on the one hand, and the sacculus on the other. Throughout the series of the vertebrates



Fig. 171. — Model of the auditory labyrinth of the left side of a chick of 7 days and 17 hours. A. Median view. B. External view. (After Rothig and Brugsch.) A. a., Ampulla of the anterior semicircular canal. A. p., Ampulla

of the posterior semicircular canal. C. a., Anterior semicircular

canal. C. 1., Pocket for formation of the lateral semicircular canal.

C. p., Pocket for formation of the posterior semicircular canal. Sa.,

Sacculus. Other abbreviations as before.

the structure of the pars superior is very uniform; the pars inferior, on the other hand, has a characteristic structure in each class and exhibits in general a progressive evolution. The condition in the chick is characteristic on the whole for the class of birds. At six days the lower division of the otocyst has grown out ventralward into a deep pouch which is curved posteriorly and towards the middle line (Fig. 170); the terminal portion is the nicUment of the lagena, and the intermediate portion of the ductus


294


THE DEVELOPMENT OF THE CHICK


cochlearis; the tip of the lagena in its growth ventralward has reached the horizontal level of the notochord. The sacculus is barely indicated yet, but is clearly seen on the seventh day as a slight protuberance on the median surface of the uppermost part of the pars inferior; it lies in front of the lower end of the endolymphatic duct at a slightly lower level and is separated by two depressions above and below, from the anterior ampulla and the ductus cochlearis respectively. The furrows above the sacculus and below the ampulla of the frontal semicircular canal mark the boundary between the pars superior and inferior.



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right side of a chick embryo of 8 days and 17

hours ; external view. (After Rothig and Brugsch.)

A. a., Ampulla of the anterior semicircular canal. A. 1., Ampulla of the lateral semicircular canal. A. p., Ampulla of the posterior semicircular canal. C. a., Anterior semicircular canah C. 1., Lateral semicircular canal. C. p., Posterior semicircular canal. Sa. e., Endolymphatic sac. U., Utriculus. Other abbreviations as before.


A day later (Fig. 172), these furrows have cut in deeper and have become continuous on the median surface; the lagena has enlarged distally, and the sacculus is a hemispherical protuberance. The tip of the lagena lies beneath the hind-brain (Fig.


ORGANS OF SPECIAL SENSE


295


168). The condition shown in Fig. 173, at eleven days seventeen hours is substantially the same as in the adult.

(d) Development of the Auditory Nerve and Sensory Areas of the Labyrinth. During the changes in the form of the labyrinth described in the preceding section, the lining epithelium has become thin and flattened except in eight restricted areas: viz., the three cristce acusticce, one in each of the ampullae of the semicircular canals, the macula utriculi, the macula sacculi, the 'papilla



Fig. 173. — Model of the auditory labyrinth of the right side of a chick embryo of 11 days and 17 hours; external view. (After Rothig and Brugsch.) Abbreviations as before.

lagenoe, the papilla hasilaris and the macula neglecta. Each of these contains sensory cells ending in fine sensory hairs projecting into the endolymph, or fluid of the labyrinth, and receives a branch of the auditory nerve proceeding from the acustic ganglia. Returning to an early stage to follow the development of sensory areas and nerves, we note first that the acustic ganglion from w^hich the auditory nerve arises takes its origin from the acustico


296 THE DEVELOPMENT OF THE CHICK

facialis ganglion which lies in front of and below the center of the auditory pit. During the closure of the latter, the acustic ganglion becomes fused with part of the wall of the otocyst in such a way that it becomes impossible to tell in ordinary sections where the epithelial cells leave off and the ganglionic cells begin. This fused area may be called the auditory neuro-epithelium. At the 36 somite stage the neuro-epithelium is confined to the lower (ventral) fourth of the otocyst, covering the entire tip, the anterior face, and a small portion of the median face (cf. Fig 98). The neuro-epithelium is the source of all the sensory areas, which arise from it by growth and subdivision. The branching of the auditory nerve follows the subdivision of the neuro-epithelium.

The exact manner in which the changes take place has not been made a subject of special investigation in the chick, so far as the author knows. However, it can be said in general that there is first a partial division of the neuro-epithelium into a pars superior and a pars inferior, and that the former divides into the cristse acusticse (sensory areas of the three ampullae) and the macula utriculi, while the latter furnishes the macula sacculi, papilla basilaris and papilla lagense.

The sensory cells differentiate from the epithelium of the labyrinth, and the nerve fibers from the bipolar neuroblasts of the acustic ganglion, the peripheral process growing into the epithelium and branching between the sensory cells, while the central process grows into the brain.

(e) Bony Labyrinth, Perihjmph, etc. The loose mesenchyme that entirely surrounds the otocyst, differentiates in the course of development into the membrana propria and perilymphatic tissue of the membranous labyrinth, the perilymph and the bony labyrinth in the following manner; on the sixth day a single layer of mesenchyme cells in contact with the cells of the otocyst are arranged with their long axes parallel to the wall, and show already in places a slight fibrous differentiation. These gradually form the membrana propria, which appears on the eighth day as an extremely thin adherent layer with protruding nuclei at intervals. The mesenchyme external to this delicate layer is already differentiated on the sixth day into a perilymphatic and a procartilaginous zone; in the former the mesenchyme is of loose consistency, and in the latter zone it has become dense


ORGANS OF SPECIAL SEXSE 297

as a precursor to chondrification. The distinction between the perilymphatic and cartilaginous zones is most distinct (on the sixth day) on the median surface of the ductus cochlearis and lagena. The differentiation proceeds rapidly, however, and on the eighth day the entire membranous labyrinth is surrounded by a mass of embryonic cartilage, the foundation of the bony labyrinth, excepting around the endolymphatic duct (Fig. 168). Between the bony and membranous labyrinths is a thick layer of perih'mphatic tissue composed of very loose-meshed mesenchyme, which in the course of the subsequent development breaks down to form the perilymphatic space. Portions of the perilymphatic tissue, however, remain attached to the membranous labyrinth and form a support for its blood-vessels and nerves.

The Development of the Tubo-tympanic Cavity, External Auditory Meatus and Tympanum. These structures develop directly or indirectly from the first or hyomandibular visceral cleft and the adjacent wall of the pharynx. In a preceding chapter the early development of this cleft was described; we saw that the pharyngeal pouch forms two connections with the ectoderm, a dorsal one corresponding to a pit-like depression of the ectoderm, and a ventral one corresponding to an ectodermal furrow. The latter connection is soon lost, the ectodermal furrow slowly disappears, and the ventral portion of the pouch flattens out. In the dorsal connection, however, an opening is formed which closes on the fourth day, and the dorsal division of the pouch then frees itself from the ectoderm and expands dorsally and posteriorly until it lies between the otocyst and the ectoderm, still preserving its connection with the pharynx (Fig. 102).

(a) The Tuho-tympanic Space. The dorsal portion of the first visceral pouch forms the lateral part of the tubo-tympanic space, but the greater portion of the latter is derived from the lateral wall of the pharynx itself, immediately adjacent to the entrance into the first visceral pouch; the region concerned extends from near the anterior edge of the second visceral pouch forwards, and ends a short distance in front of the first pouch. The original transverse diameter of the pharynx in this region increases in the course of development, and a frontal partition grows across the pharynx forming a dorsal median chamber into


298


THE DEVELOPMENT OF THE CHICK


which the two tubo-tympanic cavities open. The median chamber communicates by a longitudinal slit (tubal fissure) in the

roof of the pharynx with the oral cavity (Figs. 168 and 175).

The frontal partition in question is a posterior prolongation of the palatine processes of the maxillary arch, and forms as follows: If the head of a four-day chick be halved by a sagittal plane, and the interior of the pharynx and mouth cavity be then viewed by reflected light, an elongated lobe will be seen on the median surface of the mandibular arch and maxillary process (Fig. 174 A). This lobe begins far forward on the median surface of the maxillary process and may be followed posteriorly over the median surface of the mandibular arch to the first visceral pouch, where it ends with a free rounded extremity. The lobe itself is called by Moldenhauer the colliculus palato-phar


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Fig. 174. — A. Head of a chick embryo of 4 days, halved by median section and viewed from the cut surface. (After Moldenhauer.)

B. Internal view of the pharynx of a pigeon embryo, corresponding in development to a chick of 10 days. (After Moldenhauer.)

Col. 1., Colliculus lingualis. Col. p. p., Colliculus palato-pharyngeus. Cr. i., Crus inferior. Cr. s., Crus superius. Hyp., Hypophysis. Mx., Maxilla. N'ch., Notochord. O. Ph. T., Ostium tubse pharyngae. S. P., Seessell's pocket. 2, 3, 4, Second, third, and fourth visceral arches.


yngeus; it is bounded above and below by depressions, viz., the sulcus tubo-tympanicus dorsally and the sulcus lingualis ventrally, both of which end behind


in the first visceral pouch; anteriorly the ventral furrow disappears at the margin of the mouth, and the dorsal furrow near SeessePs pocket. The maxil


ORGANS OF SPECIAL SENSE 299

lary portion of the colliculus palato-pharyngeus corresponds to the palatine processes of mammals; the mandibular portion is peculiar to Saiiropsida.

If the interior of the pharynx and oral cavity of a ten-day chick be examined (Fig. 174 B), it will be found that the colliculus has undergone important changes. Its maxillary or anterior division divides in two limbs, crura superior and inferior^ diverging anteriorly and separated by a depression which continues the nasal cavity backward; its free posterior end extends farther backwards than before, and is more elevated. The bounding sulci are both deeper than before. The sulcus tubotympanicus, with which we are specially concerned, now extends on to the median surface of the hyoid arch. Subsequently, the crura superiores of the opposite side meet in the middle line and fuse together; in a similar fashion the posterior ends of the colliculi fuse; thus the sulci tubo-tympanici open into a dorsal chamber common to both, which communicates with the ventral division of the pharynx by a slit remaining between the two fused areas. The crura inferiores also approach one another in the middle line but do not fuse, thus leaving the typical split palate of birds in front of the fused lower ends of the crura superiores. In this way the typical adult condition of the bird's palate is established.

From this description it will be seen that only the most lateral portion of the tubo-tympanic cavity is directly derived from the first visceral pouch. In later stages it is quite impossible to say exactly what part, but it is quite certain that it lies within the tympanic part of the cavity. About the end of the fifth or the beginning of the sixth day the tubo-tympanic canal begins to enlarge distally to form the tympanic cavity proper (cf. Fig. 168); the auditory ossicles (see chapter on skull) are beginning to form just above its dorsal extremity, and as the tympanic cavity enlarges it expands around them, displacing the mesenchyme, and finally meets above the auditory ossicles, so that these appear to lie within it, though as a matter of fact the relation is analogous to that of the entodermal alimentary tube to the body-cavity. The process of inclusion of the auditory ossicles is not, however, concluded until about the twelfth day. The blind end of the tympanic cavity attains a level dorsal to the external auditory meatus. (See below.)


300 THE DEVELOPMENT OF THE CHICK

During the seventh and eighth days the enlarging cartilaginous labyrinth presses down on the Eustachian tube and hinders its further enlargement. On the eighth day the tube is a wide but narrow slit which appears crescentic in a sagittal section of the head (Fig. 150).

Some rather obscure details about the formation of the tubo-tympanic canal are mentioned here as suggestions for further work on the subject. On the sixth day almost the entire roof is composed of flattened cells similar to the roof of the pharynx; the floor, however, is lined with a columnar epithelium which extends out to and surrounds the distal extremity; it seems probable that this terminal chamber lined on all sides by columnar epithelium represents the first visceral pouch proper. On the eighth day the cavity of this distal chamber is completely constricted off from the main tympanic cavity, though it is still connected with the latter by a solid rod of cells, which gives unequivocal evidence of its origin. I do not know what becomes of this separated cavity later. (See Fig. 168 X.)

(5) The External Auditory Meatus and the Tympanum. We have already seen that on the ectodermal side there are originally two depressions corresponding to the first visceral pouch, viz., a dorsal round one in which a temporary perforation is formed, and an elongated ventral furrow. Between these is a bridge of tissue within which the external auditory meatus arises as a new depression, first clearly visible on the sixth day, when it is surrounded by four slight elevations, tw^o on the mandibular and t'wo on the hyoid arch. The meatus gradually becomes deeper and tubular, mainly owdng, I think, to the elevation of the surrounding tissue, the bottom of the meatus, or tympanic plate, being held in position by the forming stapes. The meatus is directed in a general median direction Avith a slight slant dorsally and posteriorly, and the tympanic plate is placed obliquely, not opposite the lateral extremity of the tympanic cavity, but ventrally to this (cf. Fig. 168).

Even on the sixth day the position of the head of the stapes may be recognized by the density of the mesenchyme internal to the bottom of the meatus. During the seventh and eighth days the stapes becomes sharply differentiated, and the internal face of the tympanum is established in proportion as the tympanic cavity expands around the cartilage (cf. Fig. 168). Thus the tympanum is faced by ectoderm externally, by entoderm internally, and includes an intermediate mass of mesenchyme, which differentiates by degrees into the proper tympanic substances.


CHAPTER X THE ALIMENTARY TRACT AND ITS APPENDAGES

The origin of the alimentary canal and of its various main divisions and appendages has been considered in preceding chapters. The subsequent history will now be taken up in the following order:

1. The mouth and oral cavity.

2. The pharynx and its derivatives.

3. The oesophagus, stomach and intestine.

4. The liver and pancreas.

5. The respiratory tract.

The history of the yolk-sac and allantois was considered with the embryonic membranes (Chap. VH); the detailed history of the mesenteries will be taken up in connection with the body cavities (Chap. XI).

I. Mouth and Oral Cavity

The oral cavity may be defined embryologically as that part of the alimentary canal formed on the outer side of the oral plate. Anatomically, however, such a definition is unsatisfactory both because it is impossible to determine the exact location of the oral plate in late stages, and also because of the difference in extent of the ectodermal component in roof and floor of the mouth; the definitive mouth cavity includes part of the floor of the embryonic pharynx. It is, however, of interest to determine as nearly as possible the limits of the ectodermal component of the oral cavity. In the roof this is not difficult because the hypophysis, which arises just in front of the oral plate, retains its connection with the mouth cavity until definitive landmarks are formed. The median sagittal section of an eight-day chick (Fig. 148) shows that this point is situated almost immediately opposite to the glottis, that is, between the palatine and tubal fissures in the roof (cf. Fig. 175). In the floor the extent of the ectodermal component is much less. If the tongue is entirely

301


302


THE DEVELOPMENT OF THE CHICK


a pharyngeal structure (in the embryological sense) the limit of the ectoderm would lie near the angle between the tongue and the floor of the mouth. In the side walls the boundary must be near the lines uniting the dorsal and ventral points as thus determined.


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Fig. 175. — Floor and roof of the mouth of the hen. The jaw muscles were cut through on one side, the lower jaw disarticulated and the entire floor drawn back. Corn. H., Cornu of the hyoid. Fis. pal., Palatine fissure. Fis. Tub.,

Tubal fissure. Mu., cut surface of jaw muscles.

We have already considered the formation of the boundaries of the mouth (Chap. VI and Chap. VII), and of the palate (Chap. IX, page 299). These data need not be repeated, so we have left to consider only the development of the beak, egg-tooth, tongue, and oral glands.

Beak and Egg-tooth. The beak is a horny structure formed by cornification of the epidermal cells around the margins of


ALIMENTARY TRACT AND ITS APPENDAGES


303


l£.T


the mouth: the egg-tooth is a mammiform hard structure with pointed nipple (Figs. 176 and 177) situated on the dorsum of the upper jaw near its tip (cf. Fig. 150). Its function is to aid in breaking the shell-membrane and the shell itself at the time of hatching; shortly afterwards it is lost. It is, therefore, an organ concerned with a single critical event in the life of the individual; nevertheless fully developed like the instinct of its use, needed only for the same critical event. Though its structure is different from that of the beak, it develops in connection with the latter, and the two will, therefore, be con


■s^


Fig. 176. — Outline of the upper jaw of a chick embryo of 18 days' incubation. (After Gardiner.)

E. T., Egg tooth. L. gr., Lip groove.


sidered together.

The formation of the egg-tooth begins on the sixth day from an area situated in the middle line near the tip of the upper jaw, distinguishable in the living embryo by its opacity, which contrasts with the translucency of the surrounding parts; in profile view, the area is seen to be slightly elevated. In sections the appearance is found to be due to an accumulation of rounded ectodermal cells lying between a superficial layer of periderm of several layers of cells, and the subjacent mucous layer of the epidermis (Fig. 177). Without losing their rounded shapes this mass of cells gradually assumes the form of the egg-tooth by the fourteenth day. The overlying layer of periderm is lost during the act of hatching. During their differentiation the cells of the egg-tooth secrete an intercellular substance of horny consistency in which intercellular protoplasmic connections are found. The



Fig. 177. — Transverse section through

the upper jaw of a chick embryo of

11 days. (After Gardiner.)

E. T., Egg tooth. H. Horn. L. gr., Lip groove. Pd., Periderm. T. R., Tooth ridge.


304 THE DEVELOPMENT OF THE CHICK

protoplasm of the cell-bodies themselves becomes densely packed with granules, apparently also of a horny nature, and the boundaries of the cells and outlines of the nuclei become indistinct.

Reptiles with a horny egg-shell are provided with a true dentinal tooth on the premaxilla, which has the same function as the egg-tooth of birds and of those reptiles that have a calcareous shell (crocodiles, turtles, and Trachydosaurus). The latter is, however, as we have seen, a horny structure, and therefore not a tooth morphologically. Rose therefore proposes the term Eischwiele" for the horny toothlike structure, to distinguish it sharply from the real egg-tooth.

The formation of the upper beak begins in the neighborhood of the egg-tooth and spreads towards the tip and the angle of the mouth. Similarly, in the lower jaw the differentiation begins near the tip. It is a true process of cornification, that takes place beneath the periderm and involves many layers of cells. It is therefore preceded by a rapid multiplication of cells of the mucous layer of the epidermis. Soon after the appearance of the horn a groove appears a little distance above and parallel to the margin of the upper beak, extending from the anterior end a short distance backwards (Fig. 176). In sections, this appears as an invagination of the epidermis; a similar but shallower invagination appears on the lower beak. In the upper beak the lips of the invagination fuse together and thus close the groove; in the lower beak the groove flattens out and disappears. These grooves correspond in many respects to the grooves that form the lips of other vertebrates, and they may be interpreted as a phylogenic reminiscence of lip-formation.

Teeth. All existing species of birds are toothless, but some of the most ancient fossil birds possessed well-developed teeth; it is natural, therefore, to expect that rudiments of teeth might be found in the embryos of some existing birds. In the early part of the nineteenth century some observers interpreted papillae on the margin of the jaws of certain young birds as rudimentary teeth; these were, however, shown to be horny formations, and therefore not even remotely related to teeth. Gardiner was one of the first to call attention to a thickening of the ectoderm forming a ridge projecting slightly into the mesenchyme, just inside the margin of the jaw of chick embryos about six days old (Fig. 177). The ridge disappears shortly after cornification sets in. Gardiner discussed the possibility of this represent


ALIMENTARY TRACT AND ITS APPENDAGES 305

ing a stage in tooth formation, and rejected the interpretation. Rose, however, has found the same ridge still better developed in embryos of the tern and ostrich, and identifies it very positively with the tooth-ridge or first step in the formation of the enamel organ of other vertebrates. It seems probable that this is the case, and that in this ridge we have the very last stage of the disappearance of teeth.

The Tongue. The tongue develops from two primordia in the floor of the embryonic pharynx, one situated in front of, and the other behind the thyroid diverticulum. The former, or tuberculum impar, becomes manifest on the fourth day as a slight rounded swelling situated between the lower ends of the first and second visceral arches. The swelling is bounded behind by a groove that has the ductus thyreoglossus for its center, and in front by a shallow groove, that represents the frenulum, on the posterior margin of the mandibular arches. The second primordium, or jjars copularis, arises just behind the thyroid and includes the lower ends of the second visceral arches, a small part of the lower ends of the third, and the region between these arches. According to Kallius the tuberculum impar forms only the center of the fore part of the tongue, and the lateral parts arise from two folds that form right and left of it (lateral tonguefolds). The tuberculum impar thus expanded and the pars copularis constitute two very distinct components in the development of the tongue.

Soon after the closure of the thyroid duct the two tongue components become confluent, but the zone of junction remains visible for a long time as a groove (cf. Fig. 148). Moreover the epithelium of the forward component soon becomes thickened and stratified, while in the pars copularis the epithelium remains thin and simple for a long time. With the elongation of the jaws the tip of the tongue grows forward above the frenulum (Fig. 148) and the shape of the entire organ conforms itself to the shape of the mouth cavity.

Figure 175 shows the tongue of the adult fowl. The anterior half is pointed and horny and is bounded from the posterior half by a double crescent whose posterior convexity is beset with horny spines. It seems probable that the anterior portion is derived from the precopular part, though this has not been demonstrated by continuous observation. Cornification of the precopular part


306 THE DEVELOPMEXT OF THE CHICK

sets in about the eighth day, and the early thickening of the epitheUum of this part already referred to is undoubtedly the first stage in the process.

The development of the musculature of the tongue has not been followed. The development of the skeletal parts is considered under the head of the skeleton.

Oral Glands. The following oral glands occur in the hen: 1, lingual glands; 2, mandibular glands; 3, glands opening at the angle of the mouth; 4, palatine glands in the neighborhood of the choanse. The only account of their development known to me is the brief one of Reichel. All the glands begin as solid ingrowths of the mucosa, which may branch more or less, and secondarily acquire a lumen. Their development begins relatively late. The mandibular glands appear first on the eighth day as a series of solid ingrow^ths of the mucosa extending on both sides of the base of the tongue forward to near the mandibular symphysis. They are still mostly solid on the eleventh clay, and very slightly branched, if at all. The lingual glands arise beneath the lateral margin of the tongue and grow up on each side of the lingual cartilage towards the upper surface where they branch out. They begin to form on the eleventh day. No glands form on the upper surface of the tongue. The glands of the angle of the mouth appear on the eleventh day, in situ, as slight epithelial ingrowths. Their further history has not been followed. Anterior and posterior palatine glands can be distinguished; the first in front of the choanse, the latter at the sides of and behind the choanse. They begin to appear after the eleventh day.

II. Derivatives of the Embryonic Pharynx

The pharynx, which is such an extensive and important region of the early embryo owing to the development of the visceral arches and clefts, becomes relatively much reduced in the process of development, though of course it becomes much larger absolutely. In the adult it is a somewhat ill-defined cavity from which the oesophagus leads away posteriorly, and which is confluent with the mouth anteriorly. The tubal fissure opens in its roof and the glottis in its floor. During the course of development, however, certain more or less persistent structures form from its walls, or from the epithelium of the pouches. Although these are relatively inconspicuovis organs in the adult, they are of


ALIMENTARY TRACT AXD ITS APPENDAGES 307

considerable morphological importance, being of very ancient origin and common to the whole series of vertebrates. They are the thyroid body or gland, the thymus, the postbranchial or suprapericardial bodies, and certain epithelial vestiges.

Fate of the Visceral Clefts. The times of opening and closing of the visceral clefts have been already given (pp. 176 and 177). The later history of the first visceral pouch has been described (p. 297). The second, third, and fourth pouches retain their connections with the corresponding ectodermal grooves for a long time during the thickening of the visceral arches. The consequence is, that not only the pouches, but also the ectodermal furrows, are drawn out into long epithelial tubes, and the original closing plate is thus deeply invaginated. In the case of the second cleft the tube ruptures and begins to degenerate on the sixth day, leaving no remnants. In the case of the third and fourth clefts the ectodermal components become solid on the sixth day, and form strands (funiculi prcecervicales) connecting the entodermal pouches with the sinus cervicalis. These strands are subsequently broken through and disappear. Parts of the entodermal pouches, however, persist in the thymus, suprapericardial bodies and other epithelial remains. (See below.)

Thyroid. The thyroid sac (median thyroid of authors) loses all connection with the pharyngeal epithelium on the fourth day, and on the seventh day it becomes divided in two massive lobes placed bilaterally (see Fig. 178). These then migrate backwards on each side of the trachea towards the hinder end of the derivatives of the third visceral pouch (Verdun) and become lodged in the junction of the subclavian and common carotid arteries, where they are found in the adult just internal to the jugular vein.

The so-called lateral rudiments of the thyroid, or postbranchial bodies, are histologically entirely different from the thyroid proper. They are described below.

Visceral Pouches. The second visceral pouch leaves no derivatives in the adult; during the fourth day, however, a considerable thickening of the epithelium appears on its dorsal and posterior aspect, near its opening into the pharynx; though this disappears very soon, it may be considered to represent the thymus II of Selachia and Anura.

The third visceral pouch loses its connection with the pharynx by atrophy of its internal portion between the seventh and eighth


308


THE DEVELOPMENT OF THE CHICK


days, and its intermediate portion persists as an epithelial pocket on the ventral face of the jugular vein (Fig. 178). This pocket soon divides into dorsal and ventral moities of which the former develops into the chief part of the thymus (thymus III) and the latter into the so-called epithelial vestige III. (See below.)

The fourth visceral pouch likewise separates from the pharynx on the seventh day, and furnishes from its dorsal portion the thymus IV, and from its ventral portion epithelial vestige IV. (See below.)



Fig. 178. — The derivatives of the embryonic pharynx of the chick. (After Verdun from Maurer.)

A. Of 7 days' incubation.

B. Of 8 days' incubation.

Ep. 3, Ep. 4, Epithelial bodies derived from the third and fourth visceral pouches. J., Jugular vein, p'br (V)., Postbranchial bodies derived from the fifth visceral pouch. Ph., Pharynx. Th. 3, Th. 4, Parts of the thymus derived from the third and fourth visceral pouches respectively. T'r., Thyroid. Ill, IV, third and fourth visceral clefts.

The fifth pouch (postbranchial body) likewise becomes isolated on the seventh day as a closed vesicle; its differentiation is considered below.

The Thymus. According to the above, the thymus of the chick has a double origin on each side; the main portion (thymus III) is derived from the dorsal wall of the intermediate part of the third visceral pouch. This soon elongates to form an epithelial cord extending along the jugular vein; a smaller portion (thymus IV) of the thymus is derived from a corresponding part of the fourth visceral pouch, and fuses with thymus III (Fig. 178).


ALIMENTARY TRACT AND ITS APPENDAGES 309

In the young chick the thymus forms a voluminous tract of lobulated aspect, extending the entire length of the neck; later it atrophies and in old subjects one finds only traces of it. (Verdun.)

Epithelial vestiges are formed from the ventral wall of the intermediate portions of the third and fourth visceral pouches; these come to lie together at the hinder end of the thymus in the base of the neck. They are found in the adult near the lower pole of the thyroid (Fig. 178).

The postbranchial bodies have been called lateral rudiments of the thyroid; in their differentiation, however, they do not form thyroid tissue, but two main kinds of epithelial tissues similar to the tissues of the thymus and epithelial vestiges respectively. They are to be regarded, therefore, as a fifth pair of visceral pouches, for which there are other reasons, as we have seen before. The constituent elements, however, do not separate as in the case of the third and fourth visceral pouches, but form a rather illdefined mass situated a short distance behind the thyroid (Fig. 178).

The epithelial derivatives of the embryonic pharynx in the chick are, therefore; 1. thyroid; 2. thymus (from III, IV); 3. epithelial vestiges (from III, IV); 4. postbranchial bodies, including thymus V and epithelial vestiges V. The thyroid develops in essentially the same manner in all vertebrates. In the case of the thymus it may be said in general that more visceral pouches are concerned in the lower than in the higher vertebrates.

III. The GEsophagus, Stomach and Intestine

During the third and fourth days a very pronounced lateral curvature of the alimentary canal develops, the convexity being turned to the left and the concavity therefore to the right. The part involved extends from the posterior portion of the oesophagus to the end of the duodenum. As the duodenum is at first very short, the stomach is the part principally affected at the start. The depth of the mesogastrium (dorsal mesentery of the stomach) is considerably increased by the displacement ; in the region of the greatest curvature it descends directly in the middle line, then bends sharply to the left and is attached to the dorsal wall of the stomach; the accessory mesentery arises at the bend. (See Chap. XL) The stomach does not rotate on its long axis so as to carry the attachment of the mesogastrium to the extreme


310


THE DEVELOPMENT OF THE CHICK


left, as in mammals; in the chick the lateral bending of the stomach appears to be uncomplicated by any such rotation. The curvature leaves a large space within it to the right containing the meatus venosus and liver, in short, the entire median mass of the septum transversum.

The main divisions of the intestine are marked out by their position, size-relations and structure before the closure of the yolk-stalk; thus on the third day the oesophagus appears as a constricted portion immediately behind the pharynx, and the stomach as a spindle-shaped enlargement behind the oesophagus; the duodenum is indicated at the same time by the hepatic and



Fig. 179. — Viscera of a chick embryo of 6

days, seen from the right side. (After

Duval.)

All., Allantois. Au. r., Right auricle. B.a., Bulbus arteriosus, c. pr., Csecal processes. D. L., Loop of the duodenum. Giz., Gizzard. Lg. r., Right lung. Li., Liver. R., Rectum, t. R., Tubal ridge. V., Ventricle. W. B., Wolffian body. Y. St., Yolk stalk. X., Duodcno-jejunal flexure.


pancreatic outgrowths. The form of the intestine on the sixth day is illustrated in Figure 179. Behind the stomach, the intestine forms two loops descending ventrally. The first or duodenal loop is relatively slightly developed at this time, and forms an open curve just beneath the right lobe of the liver. Its ascending limb rises to a high dorsal position just behind the liver, and


ALIMEXTARY TRACT AND ITS APPENDAGES


311


bends sharph^ to enter the descending limb of the second loop. This bend or duodeno-jejunal flexure (X, Fig. 179) is a relatively fixed point in the growth of the intestine, and marks the boundary between the duodenum and succeeding parts of the small intestine. The second loop descends deep into the umbilical cord, and the yolk-stalk is attached to its lowermost portion. A bilateral swelling at the upper end of its ascending limb is the primordium of the caecal processes, and marks the anterior end of the large intestine, which passes in a slight curve to the cloaca. In the subsequent growth of the intestine the fixed point referred to above at the hinder end of the duodenum is held in its place, and the duodenal loop in front of it simply becomes longer



Fig. 180. — Viscera of a chick embryo of 17 days'

incubation from the right side. (After Duval.)

Am., Attachment of amnion to umbilical stalk. Li. r., 1., Right and left lobes of the liver. Pc, Pancreas. U. St., UmbiHcal stalk. Other abbreviations same as Fig. 179.

without forming secondary convolutions; the pancreas comes to lie in this loop. The second loop, on the other hand, forms numerous secondary convolutions (Fig. 180) which lie at first in the umbilical cord, but which are gradually retracted (seventeenth to eighteenth day) into the abdominal cavity.

The two intestinal caeca begin to grow out as finger-shaped processes from the swelling already referred to, about the seventh day, and rapidly attain considerable length. The large intestine elongates only about in proportion to the growth of the entire embryo.

Having thus noted the general gross anatomy of the embry


312


THE DEVELOPMENT OF THE CHICK


onic intestine, we may next note a few details concerning some of its divisions. The history of the mesenteries is considered in Chapter XI).

(Esophagus. Owing to the rapid elongation of the neck the oesophagus quickly becomes a long tube. On the sixth day its lumen becomes very narrow, and on the seventh day completely occluded immediately behind the glottis, owing to proliferation of the lining cells. On the eighth day the occluded portion


\







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-y


•-'^?':


Fig. 181. — Photograph of a transverse section through the oesophagus and trachea of an 8-day chick. Cop. H., Copula of the hyoid. (Es., (Esophagus. Tr., Trachea. Ven. jug., Jugular vein.


extends only a short distance behind the glottis: it is compressed dorso- vent rally and extended laterally throughout the occluded region (Fig. 181). On the eleventh day it is open again along its entire length. The crop arises as a spindle-shaped dilatation of the fx^sophagus at the base of the neck; on the eighth day it is about double the diameter of the parts immediately


ALIMENTARY TRACT AND ITS APPENDAGES 313

in front of and behind it (Fig. 150). No detailed account of its development exists.

Stomach. It is well known that the stomach of birds exhibits two successive divisions, the pro vent riculus and the gizzard, the former of which has a digestive function and is richl}^ provided with glands, while the latter has a purely mechanical function, being provided with thick muscular walls, within which is the compressed cavity lined on each side by tendinous plates.

On the third day of incubation, the divisions of the stomach are not recognizable, either by the form of the entire organ or by the structure of the walls. On the fifth day, however, the first indications of the formation of the compound glands of the pro vent riculus may be seen in the cardiac end; the posterior or pyloric end occupies the extreme left of the gastric curve and forms the rudiment of a blind pouch projecting posteriorly, that develops into the gizzard. On the sixth and seventh days this pouch expands farther in the same direction (cf. Fig. 179), and a constriction forms between the anterior portion of the stomach, or pro vent riculus, and the gizzard, as thus marked out. The gizzard grows out farther, to the left and posteriorly, at the same time undergoing a dorso-ventral flattening, owing to the formation of the large muscle-masses. According to this account, therefore, the. greater curvature of the gizzard would represent the original left side of the portion of the embryonic stomach from which it is derived, and the original right side would be represented by the lesser curvature.

The large compound glands of the proventriculus are indicated on the fifth or sixth days as slight depressions of the entoderm towards the mesenchyme; on the seventh day these become converted into saccular glands with narrow necks (Fig. 182). Each sacculus becomes multilobed about the twelfth or thirteenth days, and each lobulus includes a small number of culs-de-sac, lined with a simple epithelium. The last subsequently become tul)ular, and the original sacculus then represents the common duct of a large compound gland. (See Cazin.)

The simple, tubular glands of the gizzard begin to form about the thirteenth or fourteenth day, and the lining of the gizzard is simply the hardened secretion of these glands; it is thus essentially different from cuticular and corneous structures of the surface of the body. According to Cazin, the glands of the gizzard


314


THE DEVELOPMENT OF THE CHICK


are formed as folds and culs-de-sac excavated in the thickness of the original epithelial wall, by elevations of the subjacent connective tissue. It should be noted finallv, that from the eie:hth day on, the surface of the mucosa, both in the proventriculus and in the gizzard, is covered with a thick layer of secretion; subsequently replaced in the gizzard by the corneous lining.



Fig. 182. — Photograph of a transverse section of an 8-day chick through the region of the proventriculus and tip of the heart. A. coel., Coeliac artery. A. o. m., Omphalomesenteric artery. Cav. om., Cavum omenti. Cav. pc, Pericardial cavity. Coel., Coelome. Gon., Gonad. Lig. g-h., Gastro-hepatic ligament. M. D., Miillerian duct. Mtn., Metanephros. p'c, Membranous pericardium. Pr'v., Proventriculus. S'r., Suprarenal. V. c. i., Vena cava inferior. Ven., Ventricle of heart. V. h. 1., Left hepatic vem. V. s'c, Subcardinal vein. V. umb., Umbihcal vein.

Large Intestine, Cloaca, and Anus. The cloaca of the adult is a large chamber opening to the exterior by the anus; it consists of three divisions: the proctodseum or terminal chamber is capable of being clo.sed by the sphincter muscle, the bursa Fabricii opens into its dorsal wall, and it is separated by a strong circular fold


ALIMENTARY TRACT AND ITS APPENDAGES


315


from the intermediate section of the cloaca or iirodaeum; this is a relatively short division of the cloaca which receives the renal and reproductive ducts in its dorsal wall by two pairs of openings; it is bounded from the larger anterior division, coprodseum, by a rather low circular fold; the coprodaeum passes gradually, without a sharp line of division, into the rectum.

The early embryological history of these parts has been considered in the preceding chapters. The condition on the fourth day is shown in the accompanying figure (Fig. 183) representing a


mMMMmmNhh



Fig. 183. — Median sagittal section of the hind end of a chick embryo

on the fourth day of incubation. (After Gasser from Maurer.)

All., Allantois. Am., Tail fold of amnion, cl. M., Cloacal membrane. CI., Cloaca. N'ch., Notochord. n. T., Neural tube. R., Rectum. Y. S ., Wall of yolk-sac.


sagittal section of the hind end of the embryo. The cloaca is the large terminal cavity of the intestine, closed from the exterior by the cloacal membrane, in which the entoderm of the floor of the cloaca is fused to the superficial ectoderm at the base of the tail. The line of fusion is a long, narrow median strip, extending from just below the neck of the allantois to the hinder end of the cloaca. Leading out from the cloaca ventrally, in front of the


316


THE DEVELOPMENT OF THE CHICK


cloacal membrane, is the neck of the allantois, and dorsal to this, the large intestine. Though not shown in the figure, it may be noted that the Wolffian ducts open into the cloaca behind and dorsal to the opening of the rectum.

The appearance of the cloaca in a longitudinal section does not, however, give an adequate idea of its form. The anterior portion of the cloaca which receives the rectum, stalk of the allantois and Wolffian ducts is expanded considerably in the lateral plane, and thus possesses a large cavity. The posterior




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Fig. 184. — Frontal section through the region of the

cloaca of a 5Way chick embryo.

an. F., Anal fold. B. F., Bursa Fabricii. CI., Cloaca. Coel., Coelome. Rect., Rectum. W. D., Wolffian duct. X., Posterior angle of the body-cavity; the epithelium is invaginated and folded so as to simulate a glandular structure.


portion, on the other hand, is greatly compressed laterally and the cavity is extremely narrow. During the fifth day the walls of this part of the cloaca become actually fused together, and its cavity obliterated, or rendered virtual only (Fig. 184). Thus the anterior part of the cloaca is prolonged backwards by a


ALIMENTARY TRACT AXD ITS APPENDAGES 317

median plate which is continuous ventrally with the cloacal membrane.

This plate was interpreted by all the earlier observers (up to Wenckebach) as the hypertrophied cloacal membrane. It is, however, not difficult to demonstrate in good series of sections, that this is not the case; the cloacal membrane forms only a small part of this plate, and its ectodermal component is thin.

During the fifth and sixth days, vacuoles appear in the posterior and dorsal part of the fused portion of the cloaca, and these soon run together in the uppermost part, but remain as a chain of vacuoles ventrally (Fig. 184). The vacuolated portion is the primordium of the bursa Fabricii and its duct. Its cavity, which is extremely narrow and ill-defined at this time, may be regarded as a re-establishment of the cavity of the posterior division of the embryonic cloaca; its communication with the anterior portion of the cloacal cavity is soon closed.

At this stage the lining epithelium of the rectum is much thickened, and the lumen has therefore become narrow (Fig. 184).

During the seventh day the conditions change very rapidly and on the eighth day the relations are as shown in Figure 185. The anterior portion of the original cloaca, or urodseum, has become compressed in an antero-posterior direction; the allantois leads off from it anteriorly and ventrally, and the rectum with its cavity now obliterated is attached to its anterior face; the dorsal extension, above the rectum (see Fig. 185), is related to the urinogenital ducts. The bursa Fabricii has now a well-defined cavity that no longer communicates with the urodseum. The tissues surrounding the cloacal membrane have grown out to form a large perianal papilla, and the cloacal membrane is therefore invaginated; its direction also is so altered that the invaginated cavity or proctodseum now lies behind it; the bursa Fabricii is on the point of opening into the highest point of the proctodseum. Vacuolization of the tissue between the cloacal membrane and the urodasum indicates its subsequent disappearance.

At eleven days (Fig. 186) the general arrangement is essentially the same, but there are important differences in detail. The bursa Fabricii has now become a long-stalked sac, opening into the proctodseum at the level of the urodseal membrane. The latter is still quite a thick plate, but the vacuoles in it fore


318


THE DEVELOPMENT OF THE CHICK


shadow its final rupture. The lower end of the large intestine is perfectly solid, and higher up, somewhat vacuolated. (The solid stage begins on the seventh day.) The urinogenital ducts open into the urodseum above the solid end of the large intestine. It will be seen, therefore, that the urodseum is transformed into a passageway between the urinogenital ducts and the allantois, being closed anteriorly by the solid large intestine and posteriorly by the urodseal (cloacal) membrane.



Fig. 185. — Photograph of the region of the cloaca in a median sagittal

section of an 8-day chick.

All., Allantois. An., Anus. B. F., Bursa Fabricii. caud. A., Caudal artery. Int., Intestine. N'ch., Notochord. p. P., Perianal papilla. Rect., Rectum. Ur'd., Urodseum.


During the twelfth and thirteenth days, the vacuoles in the upper part of the large intestine flow together and re-establish the cavity, but the lower end still remains closed by a solid plug of cells; immediately anterior to the latter the large intestine is dilated, and this apparently corresponds to the coprodaeum of


ALIMENTARY TRACT AXD ITS APPENDAGES


319


the adult cloaca. Even on the seventeenth day the large intestine appears to be still closed at its lower end, and the urodseal membrane still persists as a plug of vacuolated cells. (Gasser.) Both plugs must, however, disappear soon after.

It would thus appear that the urodgeum only of the adult cloaca corresponds to the embryonic cloaca; the proctodjeum is certainly derived from an ectodermal pit, and it is probable that



Fig. 186. — Chick embryo of 11 days, sagittal section

through the region of the cloaca. Reconstructed from

several sections. (After Minot.)

All'., Ascending limb of the allantois. AH"., Descending limb of the allantois. An., Anal invagination. An.pl., Urodeal membrane. Art., Umbihcal artery. B. F., Bursa Fabricii. b. f., Duct of the bursa. Clo., Cloaca. Ec, Ectoderm. Ent., Entoderm of the rectum. Ly., Nodules of crowded cells, probably primordia of lymphoid structures in the wall of the large intestine. W. D., Wolffian duct.

the coprodseum represents the enlarged lower extremity of the embryonic large intestine. The bursa Fabricii is an entodermal structure derived from the posterior portion of the embryonic cloaca.


IV. The Development of the Liver axd Paxcreas

The Liver. The anterior and posterior liver diverticula, described in Chapter VI, constitute the rudiments from which the


320


THE DEVELOPMENT OF THE CHICK


substance of the liver is derived. A third diverticulum is distinguished by Brouha as the right posterior diverticulum; this is an early outgrowth of the posterior diverticulum. Hepatic cylinders arise from both primary diverticula at an early stage, and these, branching and anastomosing, soon form a basket-work of liver tissue around the intermediate portion of the meatus venosus. The anterior diverticulum alone extends forward to the anterior



'M.


Fig. 187. — Reconstruction of gizzard, duodenum,

and hepato-pancreatic ducts of a chick embryo

^ of 124 hours. (After Brouha.)

D. ch., Ductus choledochus. D. cy., Ductus cysticus. D. h. cy., Ductus hepato-cysticus. D. h. d., Dorsal or hepato-enteric duct. Du., Duodenum. G. bl., Gall bladder. Giz., Gizzard. Pa. d., Dorsal pancreas. Pa. v. d.. Right ventral pancreas. Pa. V. s., Left ventral pancreas.


end of the meatus, and it even encroaches on the sinus venosus, as we have already seen; in the posterior part of the meatus venosus, on the other hand, the liver tissue is derived entirely from the posterior diverticulum. The mesenchyme in the interstices of the hepatic framework is replaced almost immediately by blood


ALIMENTARY TRACT AND ITS APPENDAGES 321

vessels that empty into the meatus, and thus appear as branches of the latter.

The gall-bladder is a very early formation, arising from the hindermost portion of the posterior hepatic diverticulum, as a distinct bud about the stage of 68 hours (Fig. 103), and forming a pyriform appendage at 84 hours. It may reasonably be regarded as derived from the most posterior portion of the primitive hepatic gutter, an interpretation that agrees with the condition found in more primitive vertebrates.

At the stage of 68 hours (cf. Fig. 103B), the anterior and posterior diverticula proceed from a common depression of the ventral wall of the duodenum, the ductus choledochus. By means of an antero-posterior constriction, the latter becomes much more clearly defined as development proceeds (Fig. 187); there arise from it also the right and left ventral primordia of the pancreas (see below), so that it receives at this stage four main ducts, viz.: the right and left ventral pancreatic diverticula and the cephalic and caudal hepatic diverticula. On the sixth day these four ducts obtain independent openings into the duodenum and the common bile duct thus ceases to exist. The relations thus established are practically the same as in the adult.

As the caudal hepatic diverticulum grows out it carries the attachment of the gall-bladder with it, so that the latter is then attached to the caudal diverticulum, which is thus divided in two parts, a distal or ductus hepato-cysticus, and a proximal or ductus cystico-entericus. That portion of the liver arising from the cephalic diverticulum is thus without any connection with the gall-bladder. There seem, however, to be anastomoses between the ductus hepato-cysticus and the original cephalic duct (ductus hepato-entericus) in the adult, lying in the commissure of the liver; the embryological origin of these appears, however, to be unknown. In the course of the development, the openings of the two original ducts into the duodenum come to lie side by side instead of one behind the other, and the original cephalic duct (ductus hepato-entericus) appears to be derived mainly from the left lobe, and the ductus cystico-entericus mainly from the right lobe of the liver. The actual distribution is, however, by no means so simple; the mode of development of the lobes of the liver (see below) would explain a preponderant dis


322 THE DEVELOPMENT OF THE CHICK

tribution of the cephalic duct to the left, and the caudal duct to the right lobe.

The liver is primarily an unpaired median organ. Its division into right and left lobes is therefore secondary and has no fundamental embryological significance. The factors that determine its definitive external form are the following: (a) the relative power of growth of its various parts; (6) limitation of its extension to the septum transversum and its connections; (c) the limitations of space in the coelome.

Bearing these principles in mind, the growth of the liver may be described as follows: three primary divisions succeeding one another in a cranio-caudal direction, may be distinguished at an early stage, viz., an antero-dorsal division, abutting on the postero-dorsal part of the sinus venosus, formed by the anterior end of the cephalic hepatic diverticulum; an intermediate division, surrounding the meatus venosus in which both cephalic and caudal hepatic diverticula are concerned; and a postero- ventral division, beneath the posterior end of the meatus venosus and the right omphalomesenteric vein, formed exclusively by the caudal diverticulum.

The growth of the liver causes expansion of the median mass of the septum transversum in all directions, excepting anteriorly, and the substance of the liver extends more or less into all the connections of the latter, viz., the lateral mesocardia, the lateral closing plates associated with the umbilical veins, the primary ventral ligament, the mesentery of the vena cava, the gastrohepatic ligament, and that part of the hepatic portal vein formed by the right omphalomesenteric vein.

At the stage of 96 hours the anterior division spreads out in the lateral mesocardia behind the Cuvierian ducts nearly to the lateral body-wall on each side. The intermediate division, on the other hand, lies largely on the right side of the middle line, owing to the displacement of the stomach to the left and the meatus venosus to the right. A small lobe is, however, pushing itself to the left beneath the gastro-hepatic ligament. The posterior division lies entirely on the right ventral side of the hinder end of the meatus venosus and right omphalomesenteric vein, as far back as the dorsal anastomosis. There are, of course, no sharp lines of demarcation between the divisions, so that in general it may be said that the liver substance tends more and


ALIMENTARY TRACT AND ITS APPENDAGES 323

more to the right side of the body from its fairly symmetrical anterior end backwards.

The lines of development of the liver are thus marked out. On the sixth day the anterior division is larger on the left than on the right side, owing no doubt to the incorporation of the sinus venosus into the right auricle, thus leaving more room for the liver on the left side. Passing backwards in a series of sections to the region of the center of the meatus venosus, we find the liver larger on the right than on the left side, being centered around the meatus, but a small lobe extends over to the left side A^entral to the stomach. The posterior division, again, is confined to the right side and ends in a free right lobe projecting caudally to the region of the umbilicus. The division of the liver into right and left lobes thus takes place on each side of its primary median ligaments, dorsal or gastrohepatic, and primary ventral; expansion being inhibited in the median line by the stomach above and heart below, it takes place on both sides, but particularly on the right side where there is more space.

The reader is referred to Chapter XI for description of the origin of the ligaments of the liver and the relations of the liver to the pericardium and other structures; also to Chapter XII for description of its blood-vessels.

The histogenesis of the liver should be finally referred to. This organ is remarkable in possessing no mesenchyme in the embryonic stages (Minot, 1900); but from the start the hepatic cylinders are directly clothed with the endothelium of the bloodvessels, so that only the thickness of the endothelial wall separates the hepatic cells from the blood in the sinusoids. The hepatic cylinders have been described as arising in the form of solid buds from the primary diverticula; the buds first formed branch repeatedly, forming solid buds of the second, third, etc., orders, and wherever buds come in contact they unite, forming thus a network of solid cylinders of hepatic cells. The solid stage does not, however, last very long, for on the fifth day it can be seen that many of them have developed a small central lumen by displacement of the cells. Thus there gradually arises a network of thick-walled tubes instead of solid cylinders, and the whole system opens into the primary diverticula from which it arose.

The Pancreas. The pancreas arises as three distinct entodermal diverticula, the origin of which has been already described, and


324


THE DEVELOPMENT OF THE CHICK


has correspondingly in the adult three separate ducts oj^ening into the duodenum. (Two pancreatic ducts is the rule in Gallus, according to Gadow in Bronn's Thierreich.) Of the three pancreatic diverticula, the dorsal one arises first (about 72 hours) then the right ventral slightly earlier than the left ventral (about 96 hours). The two latter arise from the common


cav./^.


■Pe.d.


Coel.



Goel.


^Jie/>.2d


D-Jiej) 2.


V.o.m.s.


Fig. 188. — Transverse section through the duodenum and hepatopancreatic ducts of a chick embryo of 5 days. (After Choronschitzky.) Ao., Aorta, cav. F., Caval fold. Coel., Coelome. D. hep. 2, 2 a, 2 b, Posterior hepatic diverticulvun and branches of same. Du., Duodenum. Li., Substance of Hver. M'st., Dorsal mesentery. Pa. d., Dorsal pancreas. Pa. v. d.. Right ventral pancreas. Pa. v. s., Left ventral pancreas. Spl., Spleen. V. c. p., Postcardinal vein. V. H., Vena lienalis. V. o. m. d.. Right omphalomesenteric vein. V. o. m. s., Left omphalomesenteric vein.

hepatic diverticulum near its jimction with the duodenum (Fig. 188). The differentiation of the three parts is essentially similar, and proceeds naturally in the order of their origin. Solid buds arise from the ends of the diverticula, and these branch repeatedly in the surrounding mesenchyme, but do not anastomose; the


ALIMENTARY TRACT AND ITS APPENDAGES 325

final terminations of the buds form the secreting and the intermediate portions the various intercalated and excretory ducts that form a branching system opening into the main ducts.

The successive stages in the development of the pancreas may be stated thus (following Brouha): At 124 hours the two ventral pancreatic ducts pass anteriorly and a little to the left, crossing the cephalic hepatic duct which lies between them. They are continued into ramified pancreatic tubes which already form two considera])le glandular masses. The right ventral pancreas is united by a very narrow bridge to the dorsal pancreas, and the latter is moulded on the left wall of the portal vein, while its excretory duct has shifted on the left side of the duodenum nearer the ductus choledochus. At 154 hours the duct of the dorsal pancreas is still nearer to the others, and the three pancreatic ducts enter a single glandular mass, the dorsal portion of which, derived from the primitive dorsal pancreas, is moulded on the left wall of the portal vein, and is continued into a smaller ventral portion formed by the fusion of the two ventral pancreases..

Subsequently, the pancreatic lobes fill up the duodenal loop (Figs. 179 and 180), and elongate with this so as to extend from one end of it to the other in the adult; the three ducts open near the termination of the duodenum (end of distal limb) beside the two bile ducts.

V. The Respiratory Tract

The origin of the laryngotracheal groove and the paired primordia of the lungs w^as described in Chapter VI. At the stage of 36 somites the laryngotracheal groove includes the ventral division of the post branchial portion of the pharynx, which is much contracted laterally so as to convert its cavity into a deep and narrow groove. This communicates posteriorly with right and left finger-shaped entodermal diverticula (the entodermal lung-primordia) extending into the base of the massive pearshaped mesodermal lung-primordia attached to the lateral walls of the oesophagus. The mesodermal lung-primordia are continuous with the accessory mesenteries, as described in Chapter XI; and by them attached to the septum transversum.

Bronchi. Lungs and Air-sacs. The primitive entodermal tubes form the primary bronchi, in which two divisions may be distinguished on each side, viz: a part leading from the end of


326 THE DEVELOPMENT OF THE CHICK

the trachea to the hilum of the lung (extra-puhiionary bronchus), and its continuation within the lung, extending its entire length (mesobronchus) . All the air passages of the lung, and the airsacs, arise from the mesobronchi by processes of budding and branching, enlargement of buds to form air-sacs, and by various secondary anastomoses of branches. The mesobronchi are surrounded from the first by a thick mass of mesenchyme, covered of course towards the body cavity by a layer of mesot helium. In the early development the mesenchyme of the lung-primordia grows so rapidly as to provide adequate space for the branching of the mesobronchi entirely within the mesenchymal tissue.

Although the development of the lungs of the chick was studied by several earlier investigators, our principal reliance in this subject rests on the beautiful and complete study by Locy and his students.

We may note the general topographical development as follows: The expansion of the lungs takes place into the pleural cavities; they therefore raise themselves from their surfaces of attachment, oesophagus and pleuroperitoneal membrane, and project in all directions, but especially dorsally and anteriorly (Fig. 189). We may thus distinguish free and attached surfaces; the latter is nearly a plane surface and on the whole ventral in position, and the free arched surfaces are dorsal. However, it should be remembered that the pleuroperitoneal membrane which forms the attached surface, lies at first in a sagittal plane, and only secondarily becomes frontal. In successive stages, the attached surface of the lung (pleuroperitoneal membrane) rotates from a sagittal to an approximately frontal plane (Chap. XI). An anterior lung lobe grows out in front and dorsal to the mesobronchus, beginning at six days, and the extra-pulmonary bronchus thus acquires a ventral insertion into the lung.

Stages in the development may be described as follows: At 96 hours, the bronchi arise from the end of the trachea, ventral to the oesophagus and pass back on either side of the latter, describing near their centers a rather sharp curve that brings the dorsal ends to a higher level than the oesophagus. A very slight dilatation at the extreme end of the mesobronchus is usually interpreted as the beginning of the abdominal air-sac.


ALIMENTARY TRACT AND ITS APPENDAGES


327


At six days the mesobronchus within the hmg describes a course nearly parallel to the oesophagus as far as the middle of the lung; in this part of its course it lies near the median surface and ascends very slightly. About the middle of the lung it makes a sharp bend, and passes toward the lateral and dorsal surface of the lung; here it enters a considerable thin-walled dilatation from which it is continued straight backwards by means


-. ' m\J^!^


^^^'A/



■Nes-b.dX ^^;;^


Y.ca.


F-'\^'it


M'


vf


P6




Fig. 189. — Photograph of transverse section through the lungs of an 8-day chick embryo. A. A. d., Right aortic (systemic) arch. D. art. d., s., Right and left ductus arteriosi. Ent'b.l., Branches of first entobronchus. M. ph pc, Pleuropericardial membrane. Mes'b. d., s., Right and left mesobronchia. (Es., (Esophagus. Pc, Pericardial cavity, pi. Cav., Pleural cavity. Rec. p. e. s., Left pneumato-enteric recess. V. c. a., Anterior vense cavse.

of a second curve, and ends in the same slight thick-walled dilatation that we noted on the fourth day. There are thus three very distinct divisions of the mesobronchus which we may name the anterior, the middle, and the posterior.

Four evaginations arise on the sixth day from the mesial


328 THE DEVELOPMENT OF THE CHICK

wall of the anterior division of the mesobronchus, which is otherwise unbranched. These represent the entobronchi; they arise in antero-posterior order, and the first is therefore the largest. The part of the mesobronchus from which they arise will form the vestibulum of the adult lung.

Later on the same day the ectobronchi, six in number, begin to arise from the dorsal surface of the dilated portion of the middle division of the mesobronchus. Other independent outgrowths of the same division of the mesobronchus are the so-called laterobronchi and dorsobronchi (Locy). These four groups of out-growths may be classed as secondary bronchi (Fig. 191).

On the ninth day (Fig. 191) the first entobronchus has formed a number of branches in the anterior lobe of the lung, and two of its terminal twigs, one in the antero-dorsal, the other in the anteroventral tip of the lung, are slightly dilated and project as primordia of the cervical and interclavicular air-sacs respectively. The second entobronchus is also subdivided several times; its terminal branches extending to the dorsal surface of the lung. The third entobronchus bends ventrally, and from its base a narrow canal extends into the pleuroperitoneal membrane, where it expands into the anterior thoracic air-sac, which is much the largest of the air-sacs at this time.

Between the eighth and eleventh days, numerous tertiary bronchi (parabronchi) arise from the secondary bronchi (Fig. 190). These are considerably smaller than the tubes from which they arise, and are extremely numerous, radiating from all parts of the secondary bronchi towards the free surfaces and interior of the lungs. They are embedded in the mesenchyme of the lung, which is already marked out into areas hexagonal in cross-section, with the parabronchi in the centers, by the developing pulmonary blood-vessels.

From the twelfth to the eighteenth days parabronchi of different origin meet and fuse in a most extensive fashion, thus forming an intercommunicating net-work of tubes throughout the lung. Air-capillaries finally arise from the parabronchi in the centers of the hexagonal areas and form an anastomotic net-work arising from and surrounding the parabronchi. This completes the system of tubes arising from the secondary bronchi; but


ALIMENTARY TRACT AND ITS APPENDAGES


329


another system, that of the recurrent bronchi, develops from the air-sacs which we now go on to consider.



Ft.C.


Li Pt.C.


Fig. 190. — Transverse section through the lungs of a chick embryo of 11

a. til. A. S., Anterior thoracic air-sac. Ao., Aorta. Aur. d., s., Right and left auricles. B. d., s., Right and left ducts of Botallus. F., Feather germs. Li., Liver. P. C, Pericardial cavity, p. p. M., Pleuroperitoneal membrane. P V , Pulmonary vein. Par'b., Parabronchi. PI. C, Pleural cavity. Pt. C, Peritoneal cavity. R., Rib. Sc, Scapula. V. d., s., Right and left ventricles.

The expanding hmgs nearly fill the pleural cavities on the eleventh day. Subsequently, the pleural cavity is obliterated by fusion of the free surfaces of the lungs with the wall of the pleural cavities. Thus it happens that the dorsal surfaces of the


330


THE DEVELOPMENT OF THE CHICK


lungs of the adult have no peritoneal covering," although this is denied by other authors.

The air-sacs are terminal expansions of entobronchi or of the mesobronchus (Fig. 191). From all of them with the exception of the cervical sac there grow bronchial tubes which connect with parabronchi secondarily within the lung proper. Owing to their method of origin, and also to the fact that the current of air through them in the functional lung is from the air-sacs, these tubes are known as recurrent bronchi. The lungs of birds thus differ from


Cerir.S. -Br.


.I-CLt.TnoC -Mes.moi ^Bixt. l~Ent.2 -EntA.



BcU4--^


Dors.


---i.at.3--' — HccBr.-


-Abd,S.


Fig. 191. — The air passages of the limg of the chick early on the ninth day of incubation. A Lateral view; B. Mesial view. (After Locy and Larsell.) Abd. S., Abdominal Air-sac. Ant. Th. S., Anterior thoracic air-sac. Br., Bronchi. Cerv. S., Cervical air-sac. Dors., Dorsibronchi. Ect. 1, Ect. 2, etc., First to fourth Ectobronchi. Ent. 1, Ent. 2, etc., First to fourth Entobronchi. Lat. 3, Third laterobronchus. Lat. moi.; Mes. moi.. Lateral and mesial moieties of the interclavicular air-sac. Rec. Br., Recurrent bronchi.

those of other vertebrates in having no terminal alveoli, containing residual air; there is instead a system of communicating tubes through which the air flows.

The abdominal air-sacs do not undergo any considerable expansion until after the eighth day (cf. Fig. 191). Then they push through the hinder end of the pleuroperitoneal membrane, now fused with the lateral body- wall, and penetrate the latter just beneath the peritoneum. About the tenth day they begin to expand into the abdominal cavity just behind the liver, thus evaginating the peritoneum. The left sac is somewhat larger


ALIMENTARY TRACT AND ITS \PPENDAGES 331

than the right. The expansion goes on lapidly and by the thirteenth to the fifteenth day they have reached the hinder end of the body cavity, and have akeady expanded into it so far as to form fusions with the mesentery. Recurrent bronchi begin to develop from their base about the ninth day.

The cervical sacs appear early from an anterior branch of the first entobronchus (Fig. 191). They form no recurrent bronchi (Locy).

The interclavicular sac, which is single in the adult, arises from two sacs on each side, a lateral moiety from the first entobronchus, and a mesial moiety from the third. These four parts fuse to form the single sac of the adult (Locy). These sacs form recurrent entobranchi.

The anterior thoracic sac forms about the seventh day as a dilatation of the ventral wall of the third entobronchus projecting into the pleuroperitoneal membrane near its median edge; it thus lies just lateral to the pneumato-enteric recesses. From this position it expands laterally and posteriorly in the pleuroperitoneal membrane and thus gradually splits it in two layers (Fig. 190, 11 days).

The posterior thoracic air-sac arises from the third laterobronchus somewhat later than the others, and grows at first through the hinder portion of the pleuroperitoneal membrane to enter the lateral body wall. In its subsequent expansion, it splits the posterior portion of the pleuroperitoneal membrane, as the anterior thoracic air-sac does the anterior portion of the same membrane. Anterior and posterior thoracic air-sacs then come into contact, forming a septum. Both form recurrent bronchi.

The lower layer of the pleuroperitoneal membrane, split off from the upper layer by expansion of anterior and posterior thoracic air-sacs, constitutes the oblique septmn. The most posterior portion of the oblique septum, however, is derived from the peritoneum of the lateral body wall by expansion of the posterior thoracic air-sacs behind the pleuroperitoneal membrane.

Like the abdominal air-sacs, the remainder expand rapidly, particularly from the fourteenth day on, among the thoracic viscera, and fuse intimately with these and the walls of the body cavity in a few days, the coelomatic fluid being in the meantime absorbed. The interclavicular air-sac grows out to form the subscapular air-sac and at the time of hatching has approached close to the humerus." (Selenka.)


332 THE DEVELOPMENT OF THE CHICK

The Laryngotracheal Groove.. The embryonic primordium of the larynx and trachea communicates at first along its entire length with the postbranchial division of the pharynx (72 hours). At 96 hours the hinder portion of the groove is already converted into a tube lying beneath the anterior end of the oesophagus; this is the beginning of the trachea; the anterior part of the original groove represents the larynx, and its opening into the pharynx the glottis. It is not clear whether the trachea arises as an outgrowth of the hinder end of the laryngotracheal groove, or from the hinder portion of the groove itself, by constriction from the pharynx. At 96 hours the lumen of the lower end of the trachea and adjoining portion of the two bronchi is obliterated by thickening of the walls; this is, however, a very transitory condition.

The growth of the trachea in length is extremely rapid, keeping pace, of course, with the elongation of the neck. At six days the trachea is a long epithelial tube with thick wahs branching into the two bronchi at its lower end. At its cephahc end the lumen opens into a considerable cavity, representing the larnyx; the glottis appears to be closed by a plug of epithelial cells continuous with the sohd wall of the oesophagus. At eight days the lumen of both larynx and glottis is completely closed by the thickened epithehum; at eleven days the cavity of the lower end of the larynx is re-established, and the cell mass at the upper end is converted into a mesh-work by vacuoUzation; the lips of the glottis still show a complete epithelial fusion. Thus it is apparent that the cavity of the larynx is estabhshed by the formation of vacuoles within the soUd cell-mass, and by their expansion and fusion. I cannot say how soon the glottis becomes open.

The development of the laryngotracheal apparatus, including the cartilages and muscles, has not been specially investigated in the chick. In general, it can be said that the parts external to the epithehum arise from the mesenchyme, which begins to condense around the epithelial tube on the fifth day. On the eighth day the glottis forms a decided projection into the pharynx. Distinct cartilaginous rings in the trachea are not visible on the eighth day, but are well formed on the eleventh day. As regards the syrinx it has been established by Wunderhch for Fringilla domestica that the tympanic cartilage arises from the lower tracheal rings. The origin of the musculature of the syrinx is not known.


CHAPTER XI THE BODY-CAVITIES, MESENTERIES AND SEPTUM TRANSVERSUM

The development of these parts is one of the most difficult subjects in embryologA^ involving, as it does, complex relations between the viscera, vascular system, and primitive body-cavity, on which the definitive relations of the bodv-cavities and mesenteries depend.

The pericardial and pleuro peritoneal cavities are completely separated in all vertebrates excepting Amphioxus, cyclostomes and some Selachii and ganoids, in which narrow apertures exist between the two. The pleural and peritoneal divisions of the coelome of the trunk communicate widely in amphibia; among reptiles completely closed pleural cavities are found apparently only in Crococlilia; in birds and mammals they are completely closed.

As we have seen, in the early embryo of the chick there is free communication between all parts of the body-cavity. We have to consider, therefore, (1) the separation of the pericardial and pleuro peritoneal cavities, (2) the separation of pleural and peritoneal cavities, and (3) development of the mesenteries.

I. The Separation of the Pericardial and Pleuroperi TONEAL Cavities

The pericardial cavity proceeds from the cephalic division of the primitive coelome (parietal cavity of His). We may review its primitive relations as follows (stage of 10 somites; see Chap. V) : it contains the heart which divides it into right and left parts so long as the dorsal and ventral mesocardia persist; these, however, disappear very early. Laterally, the parietal cavity communicates with the extra-embryonic body-cavity (Figs. 53 and 54) ; posteriorly it is bounded by the wall of the anterior intestinal portal (Fig. 67), on which the heart is seated like a

333


334 THE DEVELOPMENT OF THE CHICK

rider in his saddle, the body of the rider being represented by the heart, and his legs by the omphalomesenteric veins. On each side of this posterior wall the parietal cavity communicates with the coelome of the trunk. The floor of the parietal cavity comprises two parts meeting at the head-fold, the anterior part being composed of somatopleure, and the posterior part of splanchnopleure; the former is part of the definitive pericardial wall, the latter, known as the precardial plate, is provisional

(Fig! 67).

The lateral mesocardia also take part in boundmg the parietal cavity. It will be remembered that these arise as a fusion on each side between the somatopleure and the primitive omphalomesenteric veins, and that the ducts of Cuvier develop in them. As the blastoderm is spread out flat at the time that they form, they constitute at first a lateral boundary to the posterior part of the parietal cavity; but as the embryo becomes separated from the blastoderm they assume a frontal position between the sinus venosus and body-wall, tne original median face becoming dorsal and the lateral face ventral. Thus they come to form a dorsal wall for the posterior part of the parietal cavity (Fig. 119). The communication of the parietal cavity with the ccelome of the trunk is thus divided into two, known respectively as the dorsal parietal recess and the ventral parietal recess. The former is a passageway above the lateral mesocardia, communicating in front with the parietal (pericardial) cavity and behind with the trunk cavity; the latter is a communication on each side of the wall of the anterior intestinal portal ventral to the lateral mesocardia.

The completion of the posterior wall of the pericardium is brought about by the formation and development of the septum transversum.

Septum Transversum. The septum transversum arises from three originally distinct parts, viz., (1) a median mass, (2) the lateral mesocardia, and (3) lateral closing folds arising from the body-wall between the uml:)ilicus and the lateral mesocardia.

1. The median mass proceeds from the ventral mesentery of the fore-gut. The location of the heart and liver in the ventral mesentery divides it in three parts, viz., (a) a superior part, comprising the mesocardium and dorsal ligament of the liver (gastrohepatic ligament), uniting the floor of the fore-gut and


THE BODY-CAVITIES


335


the heart and Uver, (h) a median portion comprising the sinus venosus, ductus venosus and Hver, and (c) an inferior portion. Tlie superior part persists in the region of the sinus venosus and liver, and the inferior part only as the primary ventral ligament of the liver.

The median mass of the septum transversum thus includes the sinus venosus, liver, and dorsal and ventral ligaments of the liver.

At sixty hours the median mass includes chiefly the sinus and ductus venosus and their mesenteries. At eighty hours (Fig. 192) a constriction begins to appear between sinus and



Fig. 192. — Reconstruction of the septum transversum and associated mesenteries of a chick embryo of 80 hours. (After Ravn.) Ao., Aorta. Int., Intestine. Liv., Liver. PI. m'g., Plica


mesogastrica.


S.V., Sinus venosus.


ductus venosus, and the walls of the latter are expanded by the formation of liver tissue, so that the cylindrical form characteristic of sixty hours is lost, and the lateral walls of the ductus venosus bulge considerably. The continued growth of the liver causes a rapid lateral expansion of this portion of the septum transversum (Fig. 193 A).

The primary ventral ligament of the liver is included within the wall of the anterior intestinal portal up to al)out eighty hours. But, as the volk-sac shifts farther back, this ligament appears as a separate membrane (inferior part of the primary ventral


336


THE DEVELOPMENT OF THE CHICK



Fig. 193. — Reconstruction of the septum transversum and associated mesenteries of a chick embryo of 5 to 6 days. (After

Ravn.)

A. Entire.

B. After removal of the liver and sinus venosus.

A., Aorta, ac. M., Accessory mesentery. cav. F., Caval fold. coel. F., Coeliac fold. Her., Hiatus communis recessum. Int., Intestine. Lg., Lung. Liv., Liver, m. p., Pleuropericardial membrane, pvl., Primary ventral ligament of the hver. Sv., Sinus venosus.

mesentery), uniting the ventral and posterior face of the liver

to the body-wall just in front of the umbilicus (Fig. 193 A, pvl.).

For the purposes of these figures the body-wall is cut away.

Nevertheless, it can be seen that the pericardial cavity commiuii


THE BODY-CAVITIES 337

cates with the peritoneal cavity around the median mass of the septum transversum beneath the kiteral mesocardia.

2. The lateral mesocardia constitute the second component of the septum transversum. At the stage of sixty hours they are nearly round in section. At eighty-six hours the substance posterior to the duct of Cuvier begins to thicken (Fig. 192) so that the section is no longer round but elongated towards the umbilicus. They still extend almost transversely to the lateral body-wall. However, the retreat of the heart backwards soon changes their direction (Fig. 193 A) so as to form a long oblique partition between the pericardium and the dorsal parietal recess, the direction of the ducts of Cuvier being changed at the same time. The lateral mesocardia are directly continuous with the anterior portion of the median mass of the septum transversum.

3. The lateral closing folds arise as ridges of the lateral bodywall extending obliquely from the primary ventral ligament of the liver upwards and forwards to the lateral mesocardia. They arise along the course of the umbilical veins which open at first into the ducts of Cuvier. As the lateral closing folds develop first at their anterior ends, they appear as direct backward prolongations of the lateral mesocardia. They fuse with the lateral ventral surface of the liver (median mass of the septum transversum), and when they are completed back to the primary ventral ligament of the liver, they completely close the ventral communication of the pericardium with the peritoneal cavity. They mark out a triangular area on the cephalic face of the liver with postero-ventral apex and antero-dorsal base, which forms the median portion of the posterior wall of the pericardium (cf. Fig. 193 A). At six days the ventral communication of the pericardium is reduced to a very small opening, and at eight days it is entirely closed.

Closure of the Dorsal Opening of the Pericardium. As already noted the pericardial cavity communicates with the peritoneal cavity above the lateral mesocardia by way of the dorsal parietal recesses, which are destined to form a large part of the pleural cavities. We have, therefore, to consider next the closure of the aperture between the pleural and pericardial cavities. We have already seen that the heart shifts backwards very rapidly between the third and sixth days, and this draws out the lateral mesocardia in an oblique plane directed from dorsal anterior to


338 THE DEVELOPMENT OF THE CHICK

ventral posterior (Fig. 193); the ducts of Ciivier thus become oblique also, and the lateral mesocardia become converted into an oblique septum between the posterior parts of the incipient pleural cavities and the pericardial cavity (pleuro-pericardial membrane). In front of the sinus venosus, however, the pleural and pericardial cavities communicate with one another between the ducts of Cuvier, which form a projection from the lateral body-wall, and the bronchi which project laterally beneath the oesophagus. These apertures are gradually closed by fusion of the walls of the bronchi with the projecting duct of Cuvier, beginning in front and extending back to the sinus venosus. Thus the incipient pleural cavities come to end blindly in front, though they still communicate widely behind with the peritoneal cavity. The membrane thus established between pleural and pericardial cavities is know^n as the pleuro-pericardial membrane.

Establishment of Independent Pericardial Walls. With the formation of the ventral body-wall the precardial plate (a portion of the splanchnopleure, which at first forms part of the floor of the pericardial cavity) is gradually replaced by the ventral bodywall. The pericardial cavity is thus bounded ventrally and laterally by the body-wall and posteriorly by the median mass of the septum transversum. It has no independent walls at first. The definitive pericardium is, however, a membranous sac, and this is formed by two main processes: in the first place the membrane of the anterior face of the liver (median mass of the septum transversum) which forms the posterior boundary of the pericardium becomes much thickened, and gradually splits off from the liver (cf. Figs. 148 and 150), the peritoneal cavity extending pari passu between the liver and the membrana pericardiaco-peritoneale thus formed. The suspensory ligament of the liver, however, remains in the middle line, and the membrane is also directly continuous w^ith the liver dorsally around the roots of the great veins. Thus a membranous wall is established for the posterior part of the pericardium. In the second place the peritoneal cavity extends secondarily into the bodywall bounding the pericardium ventrally and laterally, and thus splits a membranous pericardial sac oE from the body-wall. In this process the liver appears to play an active role. At least its anterior lobes occupy the peritoneal spaces thus established (Fig. 194). In the mammals, on the other hand, it is the ex


THE BODY-CAVITIES


339


tension of the pleural cavities ventrally that splits the membranous pericardium from the body-wall.

Derivatives of the Septum Transversum. From the preceding account it will be seen that the following are derivatives of the septum transversum: (1) The posterior part of the pericardial membrane. (2) The pleuro-pericardial membrane. (3) The liver with its vessels and gastro-hepatic and primary ventral ligaments.



Fig. 194. — Photot;raph of a transverse section of an 8-day chick.

abd. A. S., Abdominal air-sac. A. coel., Coeliac artery. Ao., Aorta. A. o. m., Omphalomesenteric artery. Aiir. d., Right auricle. Cav. pc, Pericardial cavity. M. D., Miillerian duct. M. pc, Membranous pericardium. Msn., Mesonephros. Pr'v., Proventriculus. S., Septum ventriculorum. V. c. i., Vena cava inferior. V. h. d., Right hepatic vein. V. d., Right ventricle. V. s., Left ventricle.

(4) A small part of the heart (the sinus venosus). As regards the last, it should be noted that the anterior portion of the original septum transversum is gradually constricted from the major posterior portion and becomes established as the sinus venosus;


340 THE DEVELOPMENT OF THE CHICK

this subsequently becomes incorporated in the right auricle of the heart. (See Chap. XII).

II. Separation of Pleural and Peritoneal Cavities; Origin OF THE Septum Pleuro-peritoneale

The pleuro-peritoneal septum arises from the so-called accessory mesenteries, the origin of which must now be described. At first the septum transversum has only a median dorsal mesentery, viz., the superior part of the primary ventral mesentery that unites the septum transversum to the floor of the fore-gut, and so by way of the dorsal mesentery of the latter to the dorsal body-wall. Subsequently, however, there arises a pair of mesenteries extending from the lateral wall of the cesophagus to the septum transversum. These are the accessory mesenteries, and they arise as follows: about the sixtieth hour they appear as mesenchymatous outgrowths, forming elongated lobes, projecting from the side walls of the oesophagus opposite the hind end of the lung rudiments. The right and left lobes are practically the same size at first and they bend over ventrally and soon fuse with the median mass of the septum transversum, represented at this time by the sinus and meatus venosus (cf. Figs. 118-120, Chap. VI). Thus are produced a pair of bays of the peritoneal cavity ending blindly in front, bounded laterally by the accessory mesenteries, and in the median direction by the intestine and its mesenteries. These are the pneumato-enteric recesses.

These bays have received different names from the various authors: thus His named only the right one as recessus superior sacci omenti; the left one being practically absent in mammals; Stoss called both recessus pleuro-peritoneales ; :\Iall called them gastric diverticula; Hochstetter, recessus pulmo-hepatici ; Maurer, bursa hepatico-enterica ; Ravn, recessus superior for the right one and recessus sinister for the left. We may call them the pneumato-enteric recesses (recessus pneumato-enterici) , following Broman.

At seventy-two hours the entodermal lung-sacs extend to the base of the accessory mesenteries, ending at the anterior end of the pneumato-enteric recesses. On the left side at this time the recess is fully formed back to near the anterior end of the cephalic hepatic diverticulum, on the right side considerably farther back; that is, the accessory mesentery is already longer on the right than on the left side, and the mesenchymatous lobe


THE BODY-CAVITIES 341

from which it arises (pUca mesogastrica, Broman) can be traced back, shifting its attachment to the dorsal mesentery, as far as the anterior intestinal portal and a little farther (Fig. 192, cf. also Fig. 120).

At ninety-six hours the entodermal lung-sacs extend far into the accessory mesenteries, and thus lie laterally to the pneumatoenteric recesses. On the left side the accessory mesentery ceases opposite the tip of the lung, but on the right side it is continued back by the mesentery of the vena cava as far as the middle of the stomach, and in this region its ventral attachment is to the superior lateral angle of the liver.

The growth of the lung-sacs into the accessory mesenteries divides the latter into three parts, viz., a superior portion uniting the lung to the dorsal mesentery, a median portion enclosing the lung, and an inferior portion uniting the lung-sacs to the median mass of the septum trans versum. Now, as the liver expands laterally the ventral attachment of the accessory mesentery is carried out towards the lateral body-wall, inasmuch as its attachment is to the lateral superior face of the liver (cf. Fig. 231, Chap. XIII). Thus the accessory mesenteries are gradually shifted from their original almost sagittal plane to a plane that is approximately frontal. The developing lungs project dorsally from the accessory mesenteries, which may now be called the pleuroperitoneal membranes, into the pleural cavities (Fig. 189); and the latter communicate with the peritoneal cavity onl}^ laterally to the liver. These communications are then soon closed by a fusion betw^een the lateral edges of the pleuro-peritoneal membrane and the lateral body-wall; this fusion is not completely established on the eighth day, but it is on the eleventh day.

In reptiles and mammals the so-called mesonephric mesentery plays an important part in the closure of the pleural cavities. It arises from the apex of the mesonephros at its cephalic end, and fuses with the septum transversum. It thus forms a partition between the hinder portion of the pleural cavity and the cranio-lateral recesses of the peritoneal cavity. Subsequently, in mammals, its posterior free border fuses with the caudal bounding folds of the pleural cavity that arise as forwardly directed projections from the accessory mesentery on the right side and the wall of the stomach on the left. Hochstetter states that such a mesonephric fold is found in the chick but that it does not appear to play any essential part in the formation of the septum pleuro-peritoneale.


342 THE DEVELOPMENT OF THE CHICK

I find it in the chick as a very minute vestige at the cranial end of the mesonephros associated with the funnel of the Miillerian duct. It aids in the final closure of the pleural cavity by bridging over the narrowchink between the lateral angle of the pleuro-peritoneal membrane and the lateral body-wall. (See Bertelli, 1898.)

The oblique septum of birds arises as a layer split off from the septum pleuro-peritoneale (pulmonary aponeurosis or pulmonary diaphragm of adult anatomy) by the expansion of the anterior and posterior thoracic air-sacs within it. This mode of formation is clearly seen, particularly on the right side, in a series of transverse sections of a chick embryo of eleven days (Fig. 190). Thus the cavity between the oblique septum and the pulmonary diaphragm (cavum sub-pulmonale of Huxley) is not a portion of the bodv-cavitv and bears no relation to it. The ingrowth of muscles into the pulmonary diaphragm can be observed in the same series of sections. It begins on the tenth day according to Bertelli.

HI. The Mesenteries

The dorsal mesentery is originally a vertical membrane formed by reduplication of the peritoneum from the mid-dorsal line of the body-cavity to the intestine; mesenchyme is contained from the outset between its peritoneal layers, and serves as the pathway for the development of the nerves and blood-vessels of the intestine. In the course of development, its lower edge elongates with the growth of the intestine, and is thrown into folds, or twisted and turned with the various folds and turnings of the intestine. Detailed studies of its later development in the chick have not been published, but the principal events in its history are as follows: For convenience of description the dorsal mesentery may be divided into three portions corresponding to the main divisions of the alimentary tract, viz., an anterior division belonging to the stomach and duodenum, sometimes known as the mesogastrium; an intestinal division belonging to the second loop of the embryonic intestine that descends into the umbilicus; and a posterior division belonging to the large intestine and rectum. Inasmuch as the duodeno-jejunal flexure (Figs. 179 and 180, X) retains from an early stage a short mesenterial attachment, there is quite a sharp boundary in the chick between the first and second divisions of the dorsal


THE BODY-CAVITIES 343

mesentery. The mesogastriiim becomes modified b}- the displacement of the stomach, the outgrowth of the duodenal loop, the formation of the omentum, and by the development of the pancreas and spleen in it. (See below.)

The second division of the mesentery is related to the longest division of the intestine, but as this arises from a relatively very small part of the embryonic intestine, its dorsal attachment is short and the roots of the mesenteric arteries are grouped together. The third division is relatively long and not very deep; at its base it approaches near to the mesogastrium, to which it is attached by the root of the intermediate division.

The Origin of the Omentum (mainly after Broman). In a preceding section we saw that the accessory mesentery is continued back on the right side (at the stage of seventy-two hours) by a fold of the dorsal mesentery of the stomach known as the plica mesogastrica (Fig. 120). The stomach is already displaced somewhat to the left, hence the dorsal mesentery is bent also, and the plica mesogastrica arises from the angle of the bend (Fig. 120). The ventral mesentery of the stomach, including the meatus venosus and liver, remains in the middle line. Thus the bodv-cavitv on the right of the stomach is divided into two main divisions, viz., the general peritoneal cavity lateral to the plica mesogastrica and liver, and another cavity between the plica mesogastrica and liver on the one hand, and the stomach on the other; the latter cavity has two divisions, a dorsal one between the plica mesogastrica and upper half of the stomach (recessus mesenterico-entericus) and a ventral one between the liver (meatus venosus) and stomach (recessus hepatico-entericus), which are continued anteriorly into the pneumato-enteric recesses. Subsequently, they Ijecome entirely shut off from the peritoneal cavity, but at present (stage of Fig. 120) they communicate with it by a long fissure bounded by the accessory mesentery in front, by the plica mesogastrica above, and the meatus venosus below; this opening may be called the hiatus communis recessum; it corresponds to the foramen of Winslow of mammals (cf. Fig. 193 A).

As development proceeds, a progressive fusion of the right dorsal border of the liver with the plica mesogastrica takes place in a cranio-caudal direction, thus lessening the extent of the^ hiatus.


344 THE DEVEL0P:\IEXT OF THE CHICK

At about ninety-six hours, the pUca mesogastrica divides to form two longitudinal folds, in the lateral one of which the vena cava inferior develops (cf. Fig. 193 B) ; it is hence known as the caval fold; the more median division is the coeliac fold including the coeliac arter}^ Between them is a subdivision of the recesses known as the cavo-coeliac recess, which corresponds to the atrium burs£e omentalis of mammals. The fusion of the right lateral border of the liver continues along the course of the caval fold, and the vena cava inferior is soon completely enveloped in liver tissue. Behind the point where the vena cava inferior enters the liver, the latter fuses with the ventral edge of the right mesonephros, thus progressively diminishing the opening of the collective recesses into the peritoneal cavity. At about the one hundred and sixtieth hour, the fusion reaches the portal vein, and the recesses are thus completely shut off from the peritoneal cavity. Thus a lesser peritoneal cavity is completely separated on the right side of the body from the main cavity; and from the former both lesser and greater omental spaces develop on the right and left sides respectively of the coeliac fold. (Bursa omenti minoris and bursa omenti majoris of the bursa omentalis dextra.)

The communication of the lesser and greater omental spaces in front of the coeliac fold is closed by fusion of the latter with the right side of the proventriculus at about the one hundred and sixtieth hour, though it remains open throughout life in some birds. The two omental spaces are also elongated in a posterior direction by the caudal prolongation of the right lobe of the liver and of the gizzard respectively (Fig. 195). The lateral wall of the omentum minus is attached to the lateral dorsal border of the right lobe of the liver as already described, and it is therefore carried back by the elongation of this lobe; but as the vena cava inferior is inserted about the middle of this wall and cannot be drawn back, it results that there is a deep median indentation of the lateral wall of the omentum minus, at the bottom of which lies the vena cava inferior.

The condition of both right and left omental spaces at 154 hours is shown in Figures 195 and 196. Subsequently, about the eleventh day, the mesogastrium behind the spleen becomes perforated, and the greater omental space thus opens secondarily into the left side of the body-cavity. A true omental fold exists only for a short time in the development of the chick, and is


THE BODY-CAVITIES


345


soon taken up by the caudal elongation of the stomach. Obliteration of the cavity of the omentum by fusion of its walls takes place at its caudal end. (Broman.)

Spaces corresponding to the omental cavities are also formed on the left side of the body, but they are of much less extent. (See Fig. 196.) The communication of these spaces with the greater peritoneal cavity is not, however, shut ofT as on the right side. However, a secondary and later fusion of the left lobe of the liver with the lateral body-wall, and of the gizzard with



-rBr


Doniin


Her-


Du


-Giz


-Bomd/'


Fig. 195. — Recon.struction of the omental space of a chick embryo of 154

hours from the right side. (After Broman.)

Bomaj., Bursa omenti majoris. Bomin., Bursa omenti minoris. Du., Duodenum. Giz., Gizzard. Her., Hiatus communis recessum. oe., (Esophagus, rBr., Right bronchus. Rpedx., Right pneumato-enteric recess.


the ventral body-wall does isolate a portion of the peritoneal cavity from the remainder on the left side. Into this the pneumato- and hepato-enteric cavities of the left side open; however, it is obvious that this space is not analogous to the omental spaces on the right.

Origin of the Spleen. The spleen arises as a proliferation from the peritoneum clothing the left side of the dorsal mesentery just above the extremity of the dorsal pancreas. This proliferation forms the angle of a cranio-caudal fold of the dorsal mesentery which is caused by the displacement of stomach and intestine


346


THE DEVELOPMENT OF THE CHICK


to the left side of the body-cavity (Fig. 188), and which is exaggerated by the rapid growth of the dorsal pancreas (Choronschitzky). The spleen is thus genetically related to the wall of the great omentum, and lies outside the cavity of the latter. The cells of the spleen are proliferated from a peritoneal thickening, which may be compared in this respect to the germinal epithelium. It is recognizable at ninety-six hours, and the mass formed by its proliferation grows rapidly, forming a very considerable projection into the left side of the body-cavity above the stomach, at six days (cf. Fig. 197).


Rpesi)i



Du-^^_


R/ie>-iii


— Bomaj


Fig. 196. — The same model from the left side. (After Broman.) Hrpesin., Hiatus recessus pneumato-entericus sinister. 1. Br., Left bronchus. Pr'v., Proventriculus. Rhesin., Recessus hepatoentericus sinister. Rpesin., Right pneumato-enteric recess. Other abbreviations as in Fig. 195.

According to Choronschitzky, the peritoneal cells invade the neighboring mesenchyme, and, spreading through it, form an illdefined denser area, the fundamental tissue of which is therefore mesenchymal. The meshes of the latter are in immediate continuity with the vena lienalis, but the vascular endothelium is


THE BODY-CAVITIES


347


not continued into these meshes. Thus free embryonic cells of the primordium of the spleen enter the venous circulation directly, and become transformed into blood-corpuscles.

On account of the intimate relation between the pancreas and spleen in early embryonic stages, certain authors (see esp. Woit) have asserted a genetic connection, deriving the spleen from the pancreas. There is, however, no good evidence that the relation is other than that of propinquity.


' Gon.


A.o.fn.



Fig. 197. — Photograph of transverse section through a chick embryo of 8 days. A. o. m., Omphalomesenteric artery. Du., Duodenum. Giz., Gizzard. Gon., Gonad. II., Ihum. M. D., Miillerian duct. Pc, Pancreas. V. umb., Umbilical vein.

It should also be noted that the absence of rotation of the chick's stomach (as contrasted with mammals) and the lesser development of the great omentum appear to be the causes of the more primitive position of the spleen in birds as contrasted with mammals.


CHAPTER XII THE LATER DEVELOPMENT OF THE VASCULAR SYSTEM

I. The Heart. (For an account of the earlier development,

see Chapters V and VI.)

At the stage of seventy-two hours (Fig. 198), the ventricle consists of a posterior transverse portion and two short parallel limbs; the right limb is continuous with the bulbus arteriosus

from which it may be distinguished by a slight constriction, and the left limb with the atrium. The constriction between the latter is the auricular canal. Between the two limbs in the interior of the ventricle is a short bulbo-auricular septum separating the openings of bulbus and atrium into the ventricle. A slight groove, the interventricular sulcus, that extends backwards and to the right from the bulbo-auricular angle, marks the line of formation of the future interventricular septum (Fig. 199).

The Development of the External Form of the Heart. We have seen that in the process of development the heart shifts backwards into the thorax. The ventricle undergoes the greatest displacement, owing to its relative freedom of movement, and thus comes to lie successively to the right of, and then behind the atrium. A gradual rotation of the ventricular division on its antero-posterior axis accompanies its posterior displacement; and this takes place in such a way that the bulbus is transferred to the mid-ventral line, where it lies between the auricles (Figs.

199 and 200).

The auricles arise as lateral expansions of the atrium, the

348


Fig. 198. — Ventral view of the heart of a chick embryo of 2.1 mm. head length. (After Greil from Hochstetter.)

Atr., Atrium. B. co., Bulbus cordis, b. V., The constriction between bulbus and ventricle. C. au. v., Auriculo-ventricular canal. V., Ventricle.


LATER DEVELOPMENT OF VASCULAR SYSTEM


349


left one first at an early stage and the right one later. The left auricle is thus larger than the right for a considerable period of time in the early development. When the right auricle grows out it passes above the bulbus, which is already in process of rotation, and the two auricles then expand ventrally on each side of the bulbus. The apex of the ventricle belongs primarily to the left side and this remains obvious as long as the external interventricular groove exists. In the adult the apex of the heart belongs to the left ventricle.



Fig. 199. — Ventral view of the heart of a

chick embryo of 5 mm. head-length.

(After Masius.)

Atr. d., s., Right and left auricles. B. Co. Bulbus cordis. V. Ventricle.


The varying positions occupied by the chambers of the heart in relation to the body axes constitute a serious difficulty in describing the development. For instance, the auricular canal is at first in front of the atrium (before any bending of the heart takes place). As the ventricular loop turns backward and beneath the atrium, the auricular canal is ventral to the atrium ; and finally, as the ventricles assume their definitive position behind the auricles, the derivatives of the auricular canal (auriculo-ventricular openings) come to lie behind the atrium. In other words, the atrium rotates around a transverse axis through nearly 180 degrees in such a way that its original anterior end becomes succes


350


THE DEVELOPMENT OF THE CHICK


sively ventral and posterior. The definitive ventral surface of the heart is a cranial rather than a ventral surface during the critical period of development described below, up to eight days (cf. Figs. 148 and 150). In other words, the apex of the heart is directed ventrally rather than posteriorly, though it has a posterior inclination. For simplicity of description, however, it seems better to use the definitive orientation in the following account; that is, to regard the apex of the heart as posterior instead of ventral, and the bulbus face of the heart as ventral instead of cranial, in position.



Fig. 200. — Ventral view of the heart of a chick embryo of 7.5 mm. head-length. (After

Masius.)

Atr. d., s., Right and left auricles. B. Co., Bulbus cordis. V., Ventricle.


Division of the Cavities of the Heart. The embryonic heart is primarily a single continuous tube; during development a complex series of changes brings about its complete division into right and left sides, corresponding to the pulmonary and systemic circulations. Partitions or septa arise independently in each primary division of the cardiac tube, excepting the sinus venosus, and subsequently these unite in such a way as to make two independent circulatory systems. During this time the


LATER DEVELOPMENT OF VASCULAR SYSTE:\r 351

appropriate valves are formed. We have thus to describe the origin of three primary septa, viz., the interauricular septum, the interventricular septum, and the septum of the truncus and bulbus arteriosus. These do not, however, themselves unite directly, but are joined together by the intermediation of a fourth, large, cushion-like septum formed in the auricular canal, i.e., in the opening between the primitive atrium and ventricle.

In general it may be said that the development of the three primary septa takes place from the periphery towards the center, i.e., towards the cushion-septum of the auricular canal, and that it is practically synchronous in all three, though there is a slight precedence of the interauricular septum. During the same time the cushion-septum of the auricular canal is formed. We may then consider first the origin of these septa separately, and second their union.

(o) The Septum Trunci et Bulbi Arteriosi (Septum AorticoPulmonale). This septum divides the truncus and bulbus arteriosus into two arteries, the aorta and pulmonary artery. Three divisions may be distinguished, viz., a part in the truncus arteriosus, a part in the distal division of the bulbus extending to the place of formation of the semilunar valves, and a part in the proximal portion of the bulbus, which subsequently becomes incorporated in the ventricles. In mode of formation these are more or less independent, though they unite to form a continuous septum.

The septum of the truncus arteriosus arises on the fifth day as a complete partition extending from the cephalic border of the two pulmonary arches into the upper portion of the bulbus arteriosus; the blood current flowing through the bulbus that passes behind this partition enters the pulmonary arches exclusively, that passing in front enters the two remaining pairs of aortic arches. During the latter half of the fifth day and on the sixth day the septum of the truncus is continued into the proximal portion of the bulbus and divides it in two stems. Here, however, it co-operates with three longitudinal ridges of the endocardium of the bulbus, one of which is in the direct line of prolongation of the septum of the truncus, which therefore is continued along this one and between the other two as far as the place of formation of the semilunar valves (Fig. 201). The entire septum thus formed has a slightly spiral course, of such a nature that


352


THE DEVELOPMENT OF THE CHICK



,


. AS. So p.


/


/^


(^S)


1


w


A.Sao.p.


Fig. 201. — A. Section through the truneus arteriosus of an embryo of 5 mm. head-length. B. Section through the distal portion of the bulbus arteriosus of the same embryo. (After Greil.)

A., Aorta. P., PulmonaHs. A. S. ao


the pulmonalis, which lies dorsal to the aorta distally, is gradually transposed to its left side. The third division of the aorticpulmonary septum arises near the opening of the bulbus into the ventricle in the form of two ridges of the endocardium on the right and left sides respectively of the bulbus, the pulmonary

division lying ventral and the aortic division dorsal to the incipient partition. A third slight endocardial ridge of the proximal part of the bulbus is described (Hochstetter, Greil) at this stage, but it soon disappears. The proximal bulbus ridges may be seen on the fifth day; on the sixth day they are well formed; on the seventh day they have united to form a partition w^hich becomes continup., Plane of the septum aortico-pulmo- qus with the partition in the

nale. 1, 2, and 3, Ridges prolonging DOrtion of the bulbus.

the septum aortico-pulmonale. ^tlStai poition oi ine u.uuus.

■ Thus the separation of the aortic and pulmonary trunk is completed down to the ventricle.

The semilunar valves arise by excavation of three endocardial thickenings in each trunk formed at the caudal end of the distal division of the bulbus (Hochstetter, Greil). The origin of these thickenings is as follows. Both the aortic and pulmonary trunks receive one each of the original endocardial ridges of the distal portion of the bulbus owing to the course of the aorticpulmonary septum. Each also receives half of the ridge along which the septum of the truneus is prolonged. A third ridge arises subsequently in each between these two. A cavity then arises in each ridge and opens distally into the aorta and pulmonary artery respectively, thus forming pockets open in front. These valves are fully formed at eight days.

The aortic-pulmonary septum becomes thick early in its history and the muscular layers of the vascular trunks, which at first form a common sheath for both, gradually constrict into the septum, and separate when the constriction brings them together, so that each vessel obtains an independent muscular wall. Subsequently, a constriction extends from the outer layer


LATER DEVELOPMENT OF VASCULAR SYSTEM 353

of the truncus and bulbus along the entire length of the septum, and thus completely separates the aorta and pulmonary arteries from each other. On the eighth day each vessel has independent muscular walls, and the external constriction has made some progress.

(6) The Interventricular Septum. As noted before, the interventricular sulcus that extends from the bulbo-auricular angle towards the apex of the heart marks the line of development of the interventricular septum. The right division of the primitive ventricle is therefore continuous with the bulbus and the left with the atrium. However, the partition, bulbo-auricular septum, which at first separates the primitive right and left limbs of the ventricle, undergoes rapid reduction and becomes a mere ridge by the stage of ninety-six hours. Thus the opening of the bulbus and the auricular canal lie side by side, separated only by this slight ridge. The rotation of the ventricle brings the bulbus from the right side into the mid-ventral line so that the opening of the bulbus comes to lie ventral to the auricular canal on its right side (cf. Figs. 199 and 200).

In the interior of the heart the development of the interventricular septum is associated with the formation of the trabeculse or ramified and anastomosing processes of the myocardium that convert the peripheral part of the ventricular cavity into a spongy mass at an early stage. Along the line of the interventricular sulcus these trabeculse extend farther into the cavity than elsewhere, and become united together at their apices by a slight thickening of the endocardium, which clothes them all, thus originating the interventricular septum (Fig. 202). This process begins at the apex of the ventricle, and extends towards the base, the fleshy septum becoming gradually higher and thicker and better organized. It thus has a concave free border, directed towards the bulbo-auricular ridge and continued along both the ventral and dorsal surfaces of the ventricle. The septum develops more rapidly along the dorsal than the ventral wall and on the fifth day reaches the neighborhood of the auricular canal on this side, and unites with the right side of the fused endocardial cushions which have in the meantime developed in the latter. (See below.) Thus the interventricular foramen, or communication between the ventricles, is gradually reduced in extent and limited to the ventral anterior portion of the septum. It is never completely


354


THE DEVELOPMENT OF THE CHICK


closed, but, as we shall see later, the interventricular foramen is iitilized in connecting up the aorta with the left ventricle.

It will be seen that if the original direction of this septum, as indicated by the interventricular groove on the surface, were preserved (Fig. 199), the interventricular septum would fuse with the bulbo-auricular ridge and the right ventricle would then be continuous with the bulbus only, and the left ventricle with the atrium, and circulation of the blood would be impossible. The avoidance of this condition is due to the rotation of the bulbus by which it is brought beneath the auricular canal, and by widening of the auricular canal to the right. Thus the inter


FiG. 202. — Frontal section of the heart of a chick embryo of 9 mm. head-length. (After Hochstetter.) E. C, Median endothelial cushion. 1. E. C, Lateral endothelial cushion. S. Atr., Septum atriorum. S. v., Septum ventriculorum.


ventricular septum meets the right side of the cushion-septum and divides the auricular canal, though the opening of the bulbus remains on its right.

(c) The inter auricular septum forms at the same time as the septum between the ventricles, as a thin myocardial partition arising from the vault of the atrium between the openings of the sinus venosus and pulmonary vein; it extends rapidly with concave free border towards the auricular canal, and soon fuses


LATER DEVELOPMENT OF VASCULAR SYSTEM


355


completely along its entire free border with the endothelial cushions of the latter. It would thus establish a complete partition between the two auricles were it not for the fact that secondary perforations arise in it before its free edge meets the endothelial cushions (Fig. 203). These have the same ph^^siological significance as the foramen ovale in the mammalian heart, and persist through the period of incubation, closing soon after hatching.

(d) TheCushion-septum (Septum of the Auricular Canal). This septum completes the entire system by uniting together the three septa already considered. It forms as two cushionlike thickenings of the endothelium in the floor and roof respectively of the auricular canal (cf. Figs. 202, 203 and 204). These cushions rapidly thicken so as to restrict the center of the atrioventricular aperture, and finally, fusing together, divide the latter into two vertically-elongated apertures, right and left respectively. The time of formation of this large endocardial cushion dividing the auricular canal is coincident with the formation of the other septa.

(e) Completion of the Septa.



Fig. 203. — Reconstruction of the

heart of a chick embryo of 5.7 mm.

head-length, seen from right side.

Part of the wall of the right auricle

is cut away. (After Masius.)

B. Co., Bulbus cordis. D. C. Duct of Cuvier. E. C. d., v., Dorsal and ventral endothelial cushions. O.S.v., Opening of the sinus venosus into the right auricle. 0. 1,0. 2, Primary and secondary ostia or inter-auricular connections.

Thus bv the end of the fifth


or the beginning of the sixth day of incubation, the heart is prepared for the rapid completion of a double circulation. The embryonic circulation is never completely double, however, for the reason that the embryonic respiratory organ (allantois) belongs to the aortic system, and full pulmonary circulation does not begin until after hatching. However, between the sixth and eighth days the right and left chambers of the heart become completely separated, except that the interauricular foramina


356


THE DEVELOPMENT OF THE CHICK


remain until hatching, and serve as a passageway of blood from the right side to the left side.

The completion of the cardiac septa takes place in such a way that the aorta becomes connected with the left ventricle, the pulmonary artery remaining in connection with the right. To understand how this occurs it is necessary to remember that, although the bulbus arteriosus is primitively connected with the right side of the ventricle, the revolution of the latter has transferred the bulbus to the middle line where it lies to the right of



Fig. 204. — Reconstruction of the heart of a chick embryo of 5.7 mm. head-length. Ventral face removed; interior of the dorsal half. (After Masius.) Atr. d., s., Right and left auricles. D. C. d., s., Right and left ducts of Cuvier. E. C, Endothelial cushion, i. A. S., Interauricular septum. M. V., Opening of the meatus venosus into the sinus. S. V., Sinus venosus. V. d., s., Right and left ventricles.

the interventricular septum, and ventral to the right division of the auricular canal. The bulbo-auricular ridge thus forms the floor of this side of the auricular canal. The interventricular septum is attached to the right side of the cushion-septum and its foramen and the aperture of the bulbus lie side by side. It will also be remembered that the proximal portion of the bulbus is divided by a partition formed by right and left endocardial


LATER DEVELOPMENT OF VASCULAR SYSTEM 357

ridges, and that the aortic division of the bulbus hes above the pulmonary division, that is, next the bulbo-aiiriciilar ridge. The left bulbus ridge is thus continuous with the interventricular septum immediately beneath the foramen of the latter, and the right bulbus ridge lies on the opposite side.

The bulbus septum now becomes complete by fusion of the right and left sides. The blood from the left ventricle is then forced in each systole through the interventricular foramen and along a groove in the right side of the cushion-septum into the aortic trunk. This groove, how^ever, is open to the right ventricle also above the septum of the bulbus; but it is soon bridged over by an extension of the cushion-septum along the bulboauricular ridge as far as the right side of the septum of the bulbus; in this way the space existing between the interventricular septum and the opening of the aorta is converted into a tube, and thus the aorta is prolonged through the cushion-septum, and by way of the interventricular foramen into the left ventricle.

Fate of the Bulbus. The distal portion of the bulbus is converted into the proximal parts of the aorta and pulmonary artery. The part proximal to the semilunar valves is gradually incorporated into the ventricles, owing to extension of the ventricular cavities into its wall, and subsequent disappearance of the inner wall of the undermined part.

The Sinus Venosus. (For earlier development see Chap. VI; relation to septum trans versum. Chap. XI.)

In the course of development, the sinus venosus gradually separates from the septum trans versum, though always connected with the latter by the vena cava inferior. In early stages (up to about 24 somites) it is placed quite symmetrically behind the atrium, and extends transversely to the entrance of the ducts of Cuvier on each side. The sinu-auricular aperture is approximately in the median line at first, so that the right and left divisions of the sinus are nearly symmetrical. The condition of approximate bilateral symmetry of the sinus is, however, rapidly changed by shifting of the sinu-auricalar aperture to the right side with the outgrowth of the right auricle (24-36 somites); thus the left horn of the sinus becomes elongated; moreover, the main expansion of the sinus takes place in the region of the sinu-auricular aperture, and thus the left horn appears relatively narrow in diameter. The interauricular septum forms to the left of the sinu


358 THE DEVELOPMENT OF THE CHICK

auricular aperture (Fig. 204). At the stage of ninety-six hours the o-eneral form of the sinus is that of a horseshoe situated between the atrium and the septum trans versum; the ends of the horseshoe, or horns of the sinus venosus, are continued into the ducts of Cuvier. The sinu-auricular aperture Ues on the right, and here the cavity of the sinus is largest; the right horn of the sinus is relatively short and the left horn forms a transverse piece on the anterior face of the septum transversum, which gradually curves dorsally and enters the left duct of Cuvier.

The right and left boundaries of the sinu-auricular aperture project into the cavity of the right auricle as folds that meet below the aperture and diverge dorsally (Fig. 204), thus forming sinu-auricular valves; a special development of the muscular trabecule running along the roof of the right auricle from the angle of these valves corresponds to the septum spurium of mammalia. The sinus septum arises as a fold of the roof of the sinus between the entrance of the left horn and the vena cava inferior; it grows across the sinus into the sinu-auricular aperture and thus divides the latter (cf. Fig. 231). Subsequently, the sinus becomes incorporated in the right auricle, and the systemic veins thus obtain independent openings into the latter (see account of development of the venous system). The sinu-auricular valves disappear during this process.

II. The Arterial System

The Aortic Arches. In the Amniota six aortic arches are formed connecting the truncus arteriosus with the roots of the dorsal aorta. The first four lie in the corresponding visceral arches; the fifth and sixth are situated behind the fourth visceral pouch; the fifth is a very small and transitory vessel, the existence of which was not suspected until comparatively recently (v. Bemmelen, Boas), and the sixth or pulmonary arch was previously interpreted as the fifth. The discovery of the fifth arch has brought the Amniota into agreement with the Amphibia as regards the number and significance of the various aortic arches.

The fate of the aortic arches in the chick is as follows (see Figs. 205, 206) : the first and second arches disappear as already described (Chap. VI), and the anterior prolongation of the dorsal aort2e in front of the third arch constitutes the internal carotid; the ventral ends of the first and second arches form the external


LATER DEVELOPMENT OF VASCULAR SYSTEM


359



carotid. The third arch on each side persists as the proximal portion of the internal carotids; and the dorsal aorta ruptures on each side between the dorsal ends of the third and fourth arches. The fourth arch and the root of the dorsal aorta disappear on the left side, but remain on the right as the permanent arch of the aorta. The fifth arch disappears on both sides; the sixth arch persists throughout the period of incubation and forms an important arterial channel of the systemic circulation until hatching. Then the dorsal portion (duct of Botallus or ductus arteriosus) becomes occluded, and the remainder of the sixth arch becomes the proximal portion of the pulmonary arteries.

The details of these changes are as follows: On the third and fourth days of incubation the first and second aortic arches disappear (Fig. 102). The lower ends of these arches then appear as a branch from the base of the third arch on each side, extending into the mandible and forming the external carotid artery. The dorsal aorta in front of the third arch constitutes the beginning of the internal carotid. During the fourth day the sixth pair of aortic arches is formed behind the fourth cleft, and the origin of the pulmonary arteries is transferred to them (Fig. 102). The fifth pair of aortic arches is also formed during the fourth day (Fig. 206.) It is a slender vessel passing from near the base to near the summit of the sixth arch. As it has been entirely overlooked by most investigators, it is certain that it is of very brief duration, and it may even be entirely absent in some embryos. Apparently it has no physiological importance, and it can be interpreted only as a phylogenic rudiment.

Thus at the beginning of the fifth day the entire series of aortic arches has been formed, and the first, second, and fifth


Fig. 205. — Diagram of

the aortic arches of birds

and their fate. (After

Boas.)

Car. com., Common carotid. Car. ext., External carotid. Car. int., Internal carotid. D. a., Ductus arteriosus. L., Left. p. A., Pulmonary artery. P., Right.

1, 2, 3, 4, 5, and 6, First, second, third, fourth, fifth, and sixth aortic arches.


360 THE DEVELOPMENT OF THE CHICK

have entirely disappeared. The surviving arches are the third or carotid arch, the fourth or aortic arch, and the sixth or pulmonar}^ arch. Up to this time the development is symmetrical

on both sides of the body.

During the fifth and sixth

days the two sides become

asymmetrical, the fourth arch

becoming reduced on the left

side of the body and enlarged

on the right. Fig. 207 shows

the condition on the two sides

Fig. 206. — Camera sketch of the aortic of the body on the sixth day.

arches of the left side of a chick em- Jf the fourth arch of the two

bryo U days old. From an injected ^-^^^ ^^ compared it will be

specimen. (After Locy.) ,i . ,i ^ r.

Au 1 • +• • T?- one seen that the leit one is re Abbreviations as m h ig. 205.

duced to a very narrow rudiment which has lost its connection with the bulbus arteriosus, while on the right side it is well developed. Another important change illustrated in the same figure is the reduction of the dorsal aorta between the upper ends of the carotid and aortic arches to a narrow connection. Two factors co-operate in the diminution




Fig. 207. — Reconstruction of the aortic arches of a 6-day chick embryo from a series of sagittal sections.

A. Left side.

B. Right side.

Car. com., Common carotid. Car. ext., External carotid. Car. int., Internal carotid. D. a., Ductus arteriosus. 3, 4, and 6, Third, fourth, and sixth aortic arches.

and gradual disappearance of this part of the primitive dorsal aorta, viz., the elongation of the neck and the reduction of the blood current. It will be seen that relatively little circulation is possible in this section, because the current up the carotid


LATER DEVEL0P:\IEXT OF VASCULAR SYSTEM 361

arch turns forward and that up the aortic arch turns backward, hence there is an intermediate region of stagnation, and here the obUteration occurs.

On the eighth day the changes indicated on the sixth day are completed. The left aortic arch has entirely disappeared, and the connection between the upper ends of the carotid and aortic arches is entirely lost on both sides (Fig. 208), though lines of apparently degenerating cells can be seen between the two. On the other hand, the upper end of the pulmonary arch (duct of Botallus) is as strongly developed on both sides as the right aortic arch itself. The pulmonary artery proper is relatively very minute (Fig. 208), and it can transmit only a small


<^M



A B.

Fig. 208. — Reconstruction of the aortic arches of an 8-day embryo from a series of sagittal sections.

A. Left side.

B. Right side. . -si A. o. m., Omphalomesenteric artery. Ao. A., Aortic (systemic) arch.

Car., Carotid. D. a., Ductus arteriosus, d. Ao., Dorsal aorta, p. A., Pulmonary artery. S'cl., Subclavian artery. V., Valves of the puhnonary a,rtery.

quantity of blood; the principal function of the pulmonary arch is obviously in connection with the systemic circulation. In other words, both sides of the heart pump blood into the aorta during embryonic life; after hatching, the duct of Botallus becomes occluded as already noted, and the pulmonary circulation is then fully established.

The Carotid Arch. With the retreat of the heart into the thorax, the internal and external carotids become drawn out into long vessels extending through the neck region. The internal carotids then become approximated beneath the vertebral centra. The stem of the external carotid forms an anastomosis with the internal carotid in the mandibular region, and then disappears,


362


THE DEVELOPMENT OF THE CHICK


Car. cow


s.cl.s


so that its branches appear secondarily as branches of the internal carotid. The common carotid (car. communis) of adult anatomy is derived entirely from the proximal part of the internal carotid.

The Subclavian Artery. The primary subclavian artery arises on the fourth day from the fifteenth (eighteenth of entire

series) segmental artery of the body-wall when the wing-bud forms, and gradually increases in importance with the growth of the wdng. During the fifth day a small artery that arises from the base of the carotid arch grows backwards and unites with the primary subclavian at the root of the wing. Thus the subclavian artery obtains two roots, a primary one from the dorsal aorta and a secondary one from the carotid arch (Fig. 209). As the latter grov/s in importance the primary root dwindles and finally disappears (about the ninth day). Apparently the Crocodilia and Chelonia agree with the birds in this respect, while the other vertebrates retain the primary root.

The Aortic System includes the aortic arch and the primitive dorsal aorta



Fig. 209. — Dissection of the heart and aortic arches of a chick embryo in the latter part of the sixth day of incubation. (After Sabin.)

All., Auricle. Car. com., Common carotid. S'cl. d., s., primary and secondary subclavian artery.

3, 4, 6, Third (carotid), fourth (systemic), and sixth (puhnonary) arches.


with its branches (Fig. 216).

The segmental arteries belong to the primitive dorsal aorta; originally there is a pair in each intersomitic septum, but their fate has not been thoroughly worked out in the chick. At six days the cervical segmental arteries are united on each side by


LATER DEVELOPMENT OF VASCULAR SYSTEM 363

a longitudinal anastomosis communicating with the internal carotid in front.

The two omphalomesenteric arteries are originally independent (Chap. Y), but as the dorsal mesentery forms, they fuse in a common stem extending to the umbilicus. The anterior mesenteric artery arises from this. The coeliac and posterior mesenteric arteries arise independently from the dorsal aorta (Fig. 216).

Mesonephric arteries arise from the ventro-lateral face of the dorsal aorta and originally supply the glomeruli; they are very numerous at ninety-six hours, but become much reduced in number as the renal portal circulation develops; some of them persist as the definitive renal and genital arteries.

The umbilical arteries arise from the same pair of segmental arteries that furnishes the primitive artery of the leg. Thus on the fourth day the umbilical arteries appear as branches of the sciatic arteries; but later the umbilical arteries become much larger than the sciatic (Fig. 216). The right umbilical artery is, from the first, smaller than the left. On the eighth day its intermediate portion in the region of the neck of the allantois is much constricted, and it gradually disappears. The caudal artery is the narrow posterior extremity of the dorsal aorta behind the umbilical arteries.

I do not find a stage in the chick when the umbilical arteries unite directly with the dorsal aorta by way of the intestine and dorsal mesentery, though no doubt indirect connections exist at an early stage. In mammals (Hochstetter) the primitive umbilical artery has such a splanchnic course, but a secondary connection in the somatopleure soon replaces the primary splanchnic path.

III. The Venous System. (See Chapter VI for origin of the

first venous trunks)

We shall take up the development of the venous system in the following order: (a) the system of the anterior venae cavse (venae cavse superiores) ; (5) the omphalomesenteric and umbilical veins and the hepatic portal system; (c) the system of the inferior vena cava.

The anterior venae cavae are formed on each side b}' the union of the jugular, vertebral, and subclavian veins. The jugular is derived from the anterior cardinal veins, which extend down the neck in close proximity to the vagus nerves. The embryonic


364 THE DEVELOPMENT OF THE CHICK

history of its branches is not known in detail (see Chap. VI and Fig. 162 for the first branches). The history of the vertebral veins, which open into the jugular veins near the base of the neck, formed by union of anterior and posterior branches, is likewise unknown. Presumably they are formed in part by anastomoses between segmental veins. The subclavian vein arises primitively as a branch of the posterior cardinal vein; it receives the blood from the wing and walls of the thorax. The part of the posterior cardinal behind the entrance of the subclavian vein disappears on the sixth day, and its most proximal part represents then the anterior continuation of the subclavian vein (Fig. 216). The part of the superior vena cava proximal to the union of jugular and subclavian veins is derived from the duct of Cuvier, and on the left side also from the left horn of

the sinus venosus.

The primitive omphalomesenteric veins unite behind the sinus venosus to form the meatus venosus, around which the substance of the liver develops as described in Chapters VI and X; the union extends back to the space between the anterior and posterior liver diverticula, where the omphalomesenteric veins diverge and pass out to the yolk-sac along the margins of the anterior intestinal portal (Fig. 210 A). In the latter part of the third day (34-36 somites) an anastomosis forms between the right and left omphalomesenteric veins above the intestine just behind the dorsal pancreas, and thus establishes a venous ring around the intestine, the upper portion of which is formee*. by the anastomosis, the lower portion by the meatus venosus, and the sides by the right and left omphalomesenteric veins respectively (Fig. 210 B). Even during the formation of this first venous ring it can be seen that its left side is becoming narrower than the right side, and in less than a day it disappears completely (Fig. 210 C). Thus the blood brought in by the left omphalomesenteric vein now passes through the dorsal anastomosis to the right omphalomesenteric vein, and the latter alone connects with the meatus venosus.

While this is taking place (seventy-two to ninety-six hours) the intestine has elongated, the anterior intestinal portal has shifted backwards, and a second anastomosis is formed between the two omphalomesenteric veins ventral to the intestine and immediately in front of the intestinal portal (Fig. 210 D). Thus


LATER DEVELOPMENT OF VASCULAR SYSTEM


365


a second venous ring is established around the ahmentary canal, the lower portion of which is formed by the second anastomosis,


M^


//it.


' ■ \ Af.y.




A


Kr./ [ ^,


Ko/nX'


X ^'i/.s.


D.C. -- '



m.


n)




jy.




^ D


/r/-/




y.o..7?




/^:c.r.


Y.


Fig. 210. — Diagrams illustrating the development of the hepatic portal circulation. (After Hochstetter.)

A. About the fifty-eighth hour.

B. About the sixty-fifth hour; first venous ring formed around the intestine.

C. About the seventy-fifth hour; the left limb of the first venous ring has disappeared.

D. About the eightieth hour; the second venous ring is established.

E. About the one hundredth hour; the right limb of the second venous ring has disappeared.

F. Hepatic circulation about the one hundred and thirtieth hour, immediately before the disappearance of the intermediate portion of the meatus venosus.

a. i. p., Anterior intestinal portal. D. C, Duct of Cuvier. int., Intestine. M. V., Meatus venosus. (Es., OEsophagus. Pc, Pancreas. St., Stomach. S. v.. Sinus venosus. V. c. i., Vena cava inferior. V. h.. Hepatic veins. V. o. m.. Omphalomesenteric vein. V. r. 1, First venous ring. v. r. 2, Second venous ring. V. u. d., Right umbilical vein. V. u. s., Left umbilical vein.


366 THE DEVELOPMENT OF THE CHICK

the upper portion by the first anastomosis, and the sides by the right and left omphalomesenteric veins respectively. This ring is^lso soon destroyed, this time by the narrowing and disappearance of its right side (Fig. 210 E).

Thus at about 100 hours the condition is as follows (Fig. 210 E) : the two omphalomesenteric veins unite to form a single trunk in front of the anterior intestinal portal and ventral to the intestine (second anastomosis), the single trunk then turns to the left (left side of second ring), passes forward and above the intestine to the right side (first or dorsal anastomosis), and then farther forward on the right side of the intestine (right side of first venous ring) to enter the liver, where it becomes continuous with the

meatus venosus.

The Hepatic Portal Circulation becomes established in the following manner: The meatus venosus is primarily a direct passageway through the liver to the sinus venosus (Fig. 210 C); but, as the liver trabecule increase, more and more of the blood entering the meatus venosus is diverted into the vascular channels or sinusoids that occupy the spaces between the trabeculse. By degrees these secondary channels through the liver substance form two sets of vessels, an afferent one, branching out from the caudal portion of the meatus venosus, in which the blood is flowing into the hepatic sinusoids, and an efferent set branching from the cephalic portion of the meatus venosus in which the blood is flowing from the hepatic sinusoids into the meatus (210 D and E). By degrees the circulation through the liver substance gains in importance, and liver trabeculse grow across the intermediate portion of the meatus venosus (six to seven days cf. Fig. 216), thus gradually occluding it as a direct path through the liver (Fig. 210 F).

In this way there arises a set of afferent veins of the liver, branches of the omphalomesenteric or hepatic portal vein, and a set of efferent vessels which unite into right and left hepatic veins opening into the cephalic portion of the original meatus venosus. These veins begin to be differentiated after the one hundredth hour of incubation, and the disappearance of the intermediate portion of the meatus venosus as a direct route through the liver is completed on the seventh day.

The original hepatic portal circulation is thus supplied mainly with blood from the yolk-sac. But on the fifth day the mesen


LATER DEVELOPMEXT OF VASCULAR SYSTEM ' 367

teric vein begins to form as a small vessel situated in the dorsal mesentery and opening into the omphalomesenteric vein behind the dorsal pancreas. This vein increases in importance as the development of the viscera proceeds, and becomes the definitive hepatic portal vein; it receives branches from the stomach, intestine, pancreas, and spleen. The development of these branches proceeds "pari passu with the development of the organs from which they arise, and does not require detailed description. It should be noted, however, that part of the veins from the gizzard and proventriculus form an independent vena porta sinistra which enters the left lobe of the liver.

A distinct subintestinal vein extends forward from the root of the tail at the stage of ninety-six hours to the posterior intestinal portal, where it opens into the branch of the left omphalomesenteric vein, that extends forward from the posterior end of the sinus terminalis. This vein appears to take up blood from the allantois at an early stage. However, it disappears at about the time when the umbilical vein becomes the functional vein of the allantois. Originally it appears to open into s\Tnmetrical right and left branches of the omphalomesenteric vein that encircles the splanchnic umbilicus. The right branch is, however, much reduced at ninety-six hours (cf. Hochstetter, 1888).

The Umbilical Veins. The umbilical veins appear as vessels of the lateral body-wall opening into the ducts of Cuvier (Fig. 210 C; cf. Fig. 117); at first they show anastomoses with the latter, which, however, soon disappear. They are subsequently prolonged backwards in the somatopleure along the lateral closing folds of the septum transversum (Chap. XI). Up to the end of the third day of incubation they have no direct connection with the blood-vessels of the allantois, and function only as veins of the body-wall.

However, they obtain connection with the efferent vessels of the allantois during the fourth day, apparently by widening of parts of an intervening vascular network, and then the allantoic l)lood streams through them to the heart. The right umbilical vein disappears on the fourth day, and the left one alone persists.

In the meantime the central ends of the umbilical veins have acquired new connections. (Middle of third day. Fig. 210 D.) This takes place through the formation of anastomoses, especially on the left side, between the umbilical vein and the hepatic


368 THE DEVELOPMENT OF THE CHICK

vessels. (On the right side similar connections appear, according to Brouha, but as the entire right umbilical vein soon degenerates thev need not be considered farther.) The blood of the left umbilical vein thus divides and part flows into the duct of Cuvier by way of the original termination, and part flows through the liver into the meatus venosus. The original connection is then lost and all of the blood of the umbilical vein flows through the liver into the meatus venosus. Although the intrahepatic part is at first composed of several channels, yet the blood of the umbilical vein flows fairly directly into the meatus venosus, and thus takes no part in the hepatic portal circulation. On the eighth day the entrance of the umbilical vein into the cephalic part of the meatus venosus is still broken into several channels by liver trabeculae (Fig. 182) ; these, however, soon disappear, and the vein then empties directly into the meatus venosus, which has in the meantime become the terminal part of the inferior vena cava. As the ventral body-wall closes, the umbilical vein comes to lie in the mid-ventral line, and in its course forward it passes from the body-wall in between the right and left lobes of the liver. The stem of the umbilical vein persists in the adult, as a vein of the ventral body-wall opening into the left hepatic vein.

The System of the Inferior Vena Cava (Post-cava). The post-cava appears as a branch of the cephalic portion cf the meatus venosus, and in its definitive condition the latter becomes its cephalic segment; thus the hepatic and umbilical veins appear secondarily as branches of the post-cava. The portion of the post-cava behind the liver arises from parts of the postcardinal and subcardinal veins, and receives all the blood of the posterior portion of the body and viscera, that does not flow through the hepatic portal system. The history of the development of this vein, therefore, involves an account of (1) the origin of its proximal portion within the liver, and (2) of the transformation of the postcardinals and subcardinals.

The proximal portion of the post-cava arises in part from certain of the hepatic sinusoids in the dorsal part of the liver on the right side at about the stage of ninety hours, and in part from a series of venous islands found at the same time in the caval fold of the plica mesogastrica (Figs. 211 and 212. See Chap. XI). As the caval fold fuses Avith the right dorsal lobe of


LATER DEVELOPMENT OF VASCULAR SYSTEM


369


the liver, the venous islands flow together and establish a venous trunk extending along and within the right dorsal lobe of the liver, and opening anteriorly into the meatus venosus. At first the connection with the meatus venosus lies near the sinus venosus, but in later stages is some cUstance behind the latter. Behind the liver the dorsal attachment of the caval fold is to the ventral surface of the right mesonephros, and at this place the vena cava enters the mesonephros and connects with the subcardinal veins (cf. Fig. 182).

The latter vessels arise as a series of venous islands on the median surface of the mesonephros and lateral to the aorta on each side. Such disconnected primordia are first evident at


l>.c.s. V.u.s


^M--OCd.


V.u.d



U Mark Hill (talk)'V.c.h

Fig. 21L — A drawing of a wax reconstruction of

the veins in the region of the liver of a sparrow

embryo. Outline of the liver represented by

broken lines. Dorsal view. (After Miller.)

D. C. d., s., Right and left ducts of Cuyier.

D. v., Ductus (meatus) venosus. S. V., Sinus

venosus. V.c. i., Vena cava inferior. V. u. d.,s.,

Right and left umbilical veins.

about the seventieth hour, and soon they run together to form a longitudinal vessel on each side, which has temporary direct connections with the postcardinals (Fig. 212), replaced afterwards (fifth day) by a renal portal circulation through the substance of the mesonephros. As the subcardinal veins enlarge, they approach one another just behind the omphalomesenteric artery beneath the aorta and fuse together (sixth day. Fig. 213). In the meantime, the post-cava has become continuous with the anterior end of the right subcardinal (Fig. 213).

The venous circulation is then as follows: The blood from


370


THE DEVELOPMENT OF THE CHICK


Ucp.d.


A-o.m.



Vsc.d.


LATER DEVELOPMENT OF VASCULAR SYSTEM 371


C. V.sc.d.


V3C.S.


V.c.i.


A.OM


V.c.fi.d.


Vscd.



Fig. 213. — Reconstruction of the venous system of a chick of 5 days. Ventral view. (After Miller.) a., Mesonephric veins. Ao., Aorta. A. sc. s., Left sciatic vein. Other abbreviations as before.

the right and left postcardinal veins passes through the vascular network of the mesonephros, and empties into the subcardinal veins, from which it flows into the vena cava inferior, and so through the meatus venosus to the heart. Prior to the sixth day, however, the greater portion of the blood in tlie pos


FiG. 212. — Reconstruction of the venous system of a chick of 90 hours, ventral view. (After Miller.) A. o. m., Omphalomesenteric artery, a. sc. s.. Left sciatic artery. A. u. s., Left umbilical artery, b., Vessels enclosed within ventral side of mesonephros. V. c. p. d., s., Ri^ht and left posterior cardinal veins. V. c. i., Vena cava inferior. V. sc. d., s., Right and left subcardinal veins.


372 THE DEVELOPMENT OF THE CHICK

terior cardinals passes forward to the ducts of Cuvier without entering the mesonephric circulation. On the fifth and sixth days the cephalic ends of the postcardinals gradually dwindle and disappear (cf. Fig. 216); thus all of the blood entering the postcardinals must pass through the mesonephros to the subcardinals, which thus become efferent vessels of the mesonephros; and a complete renal-portal circulation is established.

This form of circulation continues during the period of functional activity of the mesonephroi, and as the latter gradually atrophy, the portions of the subcardinals posterior to the anastomosis gradually disappear. A direct connection between the post- and subcardinals is then established on each side, by way of the great renal veins, which have in the meantime formed in connection with the development of the kidney (Fig. 214).

The crural and ischiadic veins have, in the meantime, developed in connection with the formation of the hind limbs, as branches of the postcardinals. Thus the hinder portion of the latter becomes transformed into the common iliac veins, and at the hinder end the postcardinals form an anastomosis (Fig. 214).

IV. The Embryonic Circulation

On the fourth day the blood is driven into the roots of the dorsal aorta through three pairs of aortic arches, viz., the third or carotid, the fourth or aortic, and the sixth or pulmonary. The fifth pair of aortic arches is also functional for a time during this day, but soon disappears. The blood passing ap the third or carotid arch is directed forward through the internal and external carotid arteries to the head; that passing up the fourth and sixth arches turns backwards to enter the dorsal aorta, so that there is an intermediate area of stagnation in the roots of the dorsal aorta between the carotid and aortic arches; though this is more or less problematical, the arrangement of the vessels renders such a condition very probable. A very small proportion of the blood enters the rudimentary pulmonary arteries from the sixth arch. The blood in the dorsal aorta passes backwards and enters (1) the segmental arteries, (2) the omphalomesenteric arteries, (3) the (rudimentary) umbilical arteries, and behind the latter passes into the narrow continuation of the dorsal aortse, still separate in this region, known as the caudal arteries.

The blood is returned to the heart through the sinus venosus


LATER DEVELOPMENT OF VASCULAR SYSTEM 373



Fig. 214. — Reconstruction of the venous system of a sparrow embryo, corresponding to a chick of about 14 days. (After Miller.) V. c.i. H., Intra-hepatic part of the vena cava inferior. V Part of the vena cava inferior derived from the subcardinal vein. Genital veins. V. i. e. d., s., Riorht and left vena iliaca externa


d., s.


c. i. SC,

V. V. g.,

V. i. i.,

Right and left vena intervertebralis lum


Vena iliaca interna. V. i. 1.

balls. V. r. m. d., s., Right and left great renal veins.

almost exclusively, the pulmonary veins being very rudimentary at this stage. The veins entering the sinus venosus are the ducts of Cuvier, and the meatus venosus. The former are made up on each side by (1) the anterior cardinal vein, returning blood from the head, (2) the posterior cardinal vein returning blood from the veins of the Wolffian bodv, and the intersomitic veins, (3) the umbilical veins returning blood mainly from the body


374


THE DEVELOPMENT OF THE CHICK


wall, inasmuch as direct connection with the veins of the allantois is not yet established. The meatus venosus receives the omphalomesenteric veins, and the blood of the allantois by way of the subintestinal vein (the latter arrangement of very brief duration). Thus at this time all of the blood is mixed together in the

sinus venosus, viz., that re


A m^ CA.Q.rn.) Ao. I-!- Vsrs.


-- Vils.



ceived through the ducts of Cuvier, presumal)ly venous, and that received through the meatus venosus, presumably arterial, owing to its circulation in the superficial vascular network of the yolksac. Apparently there is no arrangement for separation or discrimination in the redistribution of the blood. But on the other hand it should be noted that most of the blood comes from the yolk-sac, owing to the slight


Vu.d. Fig. 215. — Region of the bifurcation of the post-cava in the adult fowl. Ven tral view (After Miller) development of the vessels

A.m. s. (A. o.m.), Omphalomesenteric , , , . .1 • x artery. A. i. s., Left internal iliac artery, ot the embryo at this time; V. c. i., Vena cava inferior. ^ V. i. c. d., Right common iliac vein. V. i. e. d., Right external iliac vein. V. i. i. d., Right internal iliac vein. V. i. 1. s., Left vena mtervertebralis lumbalis. V. sr. s., Left suprarenal vein. Vv. g., Genital veins. Vv. r.m., Great renal veins.


and that the blood of the embryo itself cannot be highly venous owing to the shortness of the circuit and the delicate nature of the embryonic tissues, which, no doubt, permit direct access of oxygen. On the sixth day the embryonic circulation enters on a second phase, owing to the changes in the structure of the heart and arrangement of the vessels described in detail in the preceding part of this chapter.

On the eighth day the circulation is as follows: The right and left ventricles are completely separate, and the former pumps the blood into the pulmonary trunk, the latter into the aortic trunk. The carotid arteries arise from the base of the aortic arch and convey the blood to the head, and also, by way of the sul:»clavians, to the walls of the thorax and to the wing. The left aortic arch has disappeared, and the right arch is con


LATER DE\ ELOPMEXT OF VASCULAR SYSTEM 375

tinuous with the dorsal aorta. The pulmonary trunk divides into right and left arches from which the small pulmonary artery is given off on each side, and the arch is continued without perceptible diminution in size as the ductus Botalli (ductus arteriosus) to the dorsal aorta. Thus the greater quantity of blood pumped by botli sides of the heart passes into the dorsal aorta by way of the right aortic arch, and the right and left ductus Botalli; but part of the blood from the left ventricle passes into the carotids. The main branches of the dorsal aorta are (1) coeliac, distributed to stomach and liver mainh% (2) omphalomesenteric to the 3'Olk-sac and mesentery, (3) right and left umbilical arteries (of which the left is much more important, the right soon disappearing), to the allantois and leg, (4) segmental arteries to the body-wall, (5) the caudal arteries.

The anterior venae cavae (former ducts of Cuvier) return the blood from the head, wing, and walls of the thorax to the right auricle; but owing to the formation of the sinus septum, the left vena cava opens directly into the right auricle to the left of the sinus valves, and the right one, also independently, to the right of the sinus valves. The proximal portion of the vena cava inferior is the original meatus venosus, and it receives the right and left hepatic veins, the last of w^hich receives all the blood from the allantois through the umbilical vein (original left).

There is also an hepatic portal and a renal portal circulation. The hepatic portal system is supplied with blood mainly from the yolk-sac, but also from the veins of the alimentary canal by the mesenteric vein; the latter is a relatively unimportant vessel at eight da3^s, but groW'S in importance and becomes the entire hepatic portal vein after absorption of the yolk-sac. The hepatic portal vein branches wdthin the liver into a system of capillaries which reunite to form the right and left hepatic veins. Thus all the absorbed nutrient material passes through the capillaries of the liver, where certain constituents are no doubt acted on in some important, but little understood, way.

The renal portal circulation persists through the period of functional activity of the mesonephros. The afferent vein is the posterior cardinal which is supplied by the segmental veins and the veins of the leg and tail. The blood flows through the capillaries of the mesonephros into the subcardinal veins, and


376 THE DEVELOPMENT OF THE CHICK

hence to the vena cava inferior. With the degeneration of the mesonephros, the subcardinals disappear in large part and the postcardinals then empty directly into the vena cava inferior by way of the renal veins, which have formed in the meantime. The embryonic renal portal system of birds is similar in all essential respects to the permanent system of amphibia and constitutes a striking example of recapitulation. The left auricle of the heart receives the small pulmonary veins.

Thus practically all of the blood is returned to the right auricle of the heart; a considerable part of it is diverted into the left auricle through the foramina in the septum atriorum, and thus the blood reaches both ventricles. Complete systems of valves prevent its regurgitation in any direction.

It is an interesting question to what extent the different kinds of blood received by the right auricle remain separate and receive special distribution through the body. The blood poured in by the anterior venae cavse is purely venous, and it seems probable from the arrangement of the sinus valves that it passes into the ventricle of the same side, and so into the pulmonary arch and through the ductus Botalli into the dorsal aorta, and thus in part at least to the allantois where it is oxygenated. The blood coming in through the posterior vena cava is purified and rich in nutrition, for part of it comes from the allantois, where it has been oxygenated, and part has passed through the renal portal circulation, where, no doubt, it has been purified of nitrogenous excretory matter, and the remainder is mostly from the yolk-sac and hence laden with nutrition. This blood appears to be diverted through the foramen of the septum atriorum into the left auricle, and thence to the left ventricle, and so out into the carotids and aortic arch. It would seem, therefore, to be reasonably certain that the carotids receive the purest and most nutritious blood, for the blood in the dorsal aorta is mixed with the blood from the right ventricle. There can be no reasonable doubt that the heart is a more effective organ for separate and effective distribution of the various kinds of blood received by it than this account would indicate. But further investigation is necessary to determine in what ways and to what extent this takes place.

At the time of hatching the following changes take place: the umbilical arteries and vein are obliterated in the allantois, owing to drying up of the latter; their stems remaining as relatively



Fig. 216. — Diagram of the relations of the main splanchnic blood vessels

on the sixth day of incubation.

A. c, CoeHac artery. Adv., Vena advehens. All., Allantois. A. m.. Mesenteric artery. Ao., Aorta. A. o. m., Omphalomesenteric artery. A. p., Pulmonary artery. A. sc. Sciatic artery. A. u. d.. Right umbilical artery. A. u. s., Left umbilical artery. A. V., Vitelline arteries. Car. int., Internal carotid. Car. ext.. External carotid. CI., Cloaca. D. a., Ductus arteriosus. D. v., Ductus (meatus) venosus. Int., Intestine. J. e., External jugular vein. J. i.. Internal jugular vein. Li., Liver. Scl., Subclavian artery. V. c. a.. Anterior vena cava. V. c. i.. Inferior Vena cava. V. c. p.. Posterior cardinal vein. V. m., Mesenteric vein. V. o. m., Omphalomesenteric vein. Vp., Pulmonary vein. V. s'c, Subcardinal vein. V. s'cl., Subclavian vein. V. u. (s.). Umbilical vein (left). V. V., Vitelline vein. W. B., Wolffian body. Y. S., Yolk-sac. Y. St., Yolk-stalk.


LATER DEVELOPMENT OF VASCULAR SYSTEM 377

insignificant vessels. The veins of the yolk-sac likewise disappear. The ductus arteriosus (Botalli) is obliterated on both sides, and becomes a solid cord uniting the pulmonary arteries and arch of the aorta. Thus the blood from the right ventricle is driven into the lungs, and the pulmonary artery enlarges. The foramina in the septum atriorum gradually close, and so a complete double circulation is established. The right auricle receives all the systemic (venous blood), which is then driven through the lungs by way of the pulmonary artery, and returned in an oxygenated condition through the pulmonary veins to the left auricle; thence to the left ventricle and out through the aorta into the systemic circulation again.


CHAPTER XIII

THE URINOGENITAL SYSTEM

The history of the pronephros and the origin of the mesonephros have been ah'eady described (Chap. VI). We have now to consider (1) the later history of the mesonephros, (2) the development of the metanephros or permanent kidney, (3) the development of the reproductive organs and their ducts, and (4) the development of the suprarenals. All these organs form an embryological unit, by virtue of their mode of origin and their interrelations. Thus we find that the intermediate cell-mass is significant for the development of all: its growth causes the formation of the Wolffian body, on the median face of which the gonads arise. The secreting tubules and renal corpuscles of the permanent kidney are also derivatives of the intermediate cell-mass. The Wolffian duct is derived from the same source, and by change of function becomes the vas deferens, after functioning for a while as the excretory duct of the mesonephros. Certain parts of the mesonephros also enter into the construction of the testis. And the Miillerian duct, which forms the oviduct of the female, is derived from the epithelium covering the Wolffian body.

I. The Later History of the Mesonephros In Chapter VI we traced the origin of the nephrogenous tissue, and the differentiation of the first mesonephric tubules within it. We saw that in each of the segments concerned a number of balls of cells arises by condensation within the nephrogenous tissue, and that these become converted into vesicles. We saw also that each vesicle sends out a tubular sprout from its lateral side to the Wolffian duct, with which it unites; and that its median face becomes converted into a renal corpuscle. These processes take place sucessively in antero-posterior order within the somites concerned, so that a series of stages in the development of the tubules may be studied in the same embryo. Moreover, all the tubules of a given somite do not develop simul .378


THE URIXOGEXITAL SYSTEM


379


taneously: primary tubules are formed in each somite from the most ventral portion of the nephrogenous tissue; then secondar}tubules later from an intermediate portion, and tertiary tubules later yet from the dorsal portion.

Fig. 217 represents a transverse section through the middle



^»f^^5^° v'"'it>f ^i:^j#^^'







Fig. 217. — Transverse section through the middle of the

Wolffian body of a chick embryo of 96 hours.

Ao., Aorta. Coel., Coelome. Col. T., Collecting tubule. Glom., Glomerulus, germ. Ep., Germinal epithelium. M's't., Mesentery, n. t., Nephrogenous tissue. T. 1,2, 3, Primary, secondary, and tertiary mesonephric tubules. V. c. p., Posterior cardinal vein. W. D., Wolffian duct.

of the Wolffian body at the stage of ninety-six hours, showing a primary, secondary, and tertiary tubule. The primary tubule is typically differentiated; the secondary has formed the secreting tubule and the rudiment of the renal corpuscle, but the tubule does not yet open into the Wolffian duct, though it is connected with it; the tertiary tubule is still in the vesicular stage. Some undifferentiated nephrogenous tissue remains above the rudiment of the tertiary tubule, which makes it possible that quarternarv tubules mav be formed later.

Referring still to the same figure, it will be noted that the Wolffian duct itself has formed a considerable evagination dorsomedially (collecting tubule), with which both secondary and tertiary tubules are associated as well as the undifferentiated nephrogenous tissue. Similar evaginations are formed along the entire length of the functional portion of the mesonephros.


380


THE DEVELOPxAIEXT OF THE CHICK


0(,


ov


o


Q>(


o


OO,


o


o


o


o r


o


xoz


X22


-2ZIC


22YII


Fig. 114. A.


Figs. 218 and 219 illustrate the form of these evaginations in duck embr3^os of 40 and 50 somites respectively, as they appear in reconstructions of the posterior portion of the mesonephros.

It will be seen that they gradually form sacs opening into the Wolffian duct. Subsequently, by elongating, these sacs form collecting tubules that gather up the secretions of the mesonephric tubules proper and conduct them to the Wolffian duct. These conducting tubules are stated to branch more or less; it is also said that they are more highly developed in the duck than in the chick. Felix proposes to call them mesonephric ureters.

In the case of the secondary and tertiary tubules, three parts may be distinguished : parts one and two (derived from the nephrogenous tissue) I;. o\C ^rc the renal corpuscle and secreting

tubule respectively; the third part is the collecting tubule derived by evagination from the Wolffian duct. In the case of the primary tubules, a conducting part appears to be formed secondarily, though in what way is not clear.

The formation of new tubules ceases on the fifth day, all the nephrogenous tissue being then used up. Up to the eighth day at least the tubules grow rapidly in length and become more differentiated. The result is a relatively enormous protrusion into the bodv-cavity on each side of the dorsal mesentery. Degeneration of the tubules sets in about the tenth or eleventh days, and the tissue is gradually absorbed;


2Mir




'XSKT


THE URIXOGEXITAL SYSTEM


381


this process extends over the whole of the latter period of incubation, and is completed at hatching. Parts, however, remain in the male in connection with the testis; non-functional remnants


O ^ °o o O

O.'l



' ."fi.T •-.


yxxiii


n.T.


Fig. 219. — Profile reconstruction of part of the

mesonephros and diverticulum of the ureter of

a duck embryo of 50 somites. (After Schreiner.)

CI., Cloaca. Int., Intestine. Mn. T., Meso nephric tubules, n. T., Nephrogenous tissue.

Ur Ureter W. D.. Wolffian duct.

XXXII, XXXIII, XXXIV, Somites of the same number.

may also be detected in the female (p. 401). It is difficult to state the exact period of beginning and cessation of function of the mesonephric tubules. Judging from the histological appear


PiG 918 — Profile reconstruction of part of the Wolffian duct and primordia of mesonephric tubules (represented by circles) of a duck embryo of 45 somites. (After Schreiner.) YXTV XXV etc., position of the correspondmg somites. Lines 114 A,

114 B 114 C ^represent the positions of the sections shown in these figures.


382


THE DEVELOPMENT OF THE CHICK


ances, however, it is probable that secretion begins in the tubules on the fifth day and increases in amount up to the eleventh day at least, when signs of degeneration become numerous. Presumably the functional activity diminishes from this stage on, being replaced by the secretion of the permanent kidney.


SrC:^


Gq/?.-%




Fig. 220. — Transverse section through the mesonephros

and neighboring parts of a 6-day chick, in the region of

the spleen.

Ao., Aorta, bl. V., Blood vessels (sinusoids). Caps., Capsule of renal corpuscle. Coel., Coelome. col. T., Collecting tubule. D., Dorsal. Giz., Gizzard. Glom., Glomerulus. Gon., Gonad. L., Left. Spl., Spleen. Sr. C, Cortical substance of the suprarenal, s. t., Secreting tubule. T. R., Tubal rid^e. V., Ventral. V. c. p., Posterior cardinal vein V. s'c. 1., Left subcardinal vein. W. D., Wolffian duct.

Figs. 220 and 221 represent sections through the mesonephros on the sixth and eighth days respectively (see also Fig. 222, eleven days). The renal corpuscles show the typical capsule and glomerulus, and relation to the secreting tubules. The latter are considerably convoluted on the sixth day, much more so on the eighth day. The conducting tubules can usually be distinguished by their smaller caliber and thinner walls. The Wolffian


THE URIXOGEXITAL SYSTEM


383


duct is situated near the dorso-lateral edge of the mesonephros, and the opening of a collecting tubule into it is shown in Figure 220. The renal corpuscles are situated next the median face of the Wolffian body. The space between the tubules is occupied


';7.f.o.z.


Mh'tr



-3.?V iVJ).


apmm



Gon.l


Fig. 221. — Transverse section through the metanephros, mesonephros, gonads and neighboring parts of an 8-day chick, bl. v., Blood vessels (sinusoids). B. W., Body-wall. col. T. M't'n., Collecting tubules of the metanephros. M. D., Miillerian duct. M's't., Mesentery, n. t. i. z., Inner zone of nephrogenous tissue (metanephric). n. t. o. z., Outer zone of the nephrogenous tissue. Symp. Gn., Sympathetic o^anghon of the twenty-first spinal ganglion. V. C, Centrum of vertebra. Other abbreviations as before.

almost entirely by a wide vascular network of sinusoidal character; that is, the endothelial walls of the vessels are moulded directly on the basement membrane of the tubules without any intervening connective tissue. The circulation is described in the chapter on the vascular system.


384 THE DEVELOPMENT OF THE CHICK

II. The Development of the Metaxephros or Permanent

Kidney

The metanephros or permanent kidney supplants the mesonephros in the course of development. It is derived from two distinct embryonic primordial (1) the nephrogenous tissue of the two or three posterior somites of the trunk (31 or 32 to 33), which furnish the material out of which the renal corjxiscles and secreting tubules develop; and (2) a diverticulum of the posterior portion of the Wolffian duct (Fig. 219), which develops by branching into the collecting tubules and definitive ureter. The development of the kidney takes place in a mass of mesenchyme, known as the outer zone of the metanephrogenous tissue, that furnishes the capsule and connective tissue elements of the definitive kidney, in which also the vascular supply is developed (Figs. 221 and 222). The cortical tubules of the kidney are thus derived mainly from the nephrogenous tissue, and the medullary tubules and ureter from the metanephric diverticulum.

Thus the definitive kidney is analogous in mode of development to the mesonephros, and is best interpreted as its serial homologue. This point of view may be regarded as definitely established by the work of Schreiner, to which the reader is referred for a full account of the history of the subject.

The metanephric diverticulum, or primordium of the ureter and collecting tubules, arises about the end of the fourth da}^ as a rather broad diverticulum of the Wolffian duct at the convexity of its terminal bend to the cloaca (Fig. 219). It grows out dorsally, forming a little sac, which, however, soon begins to grow forward median to the posterior cardinal vein and dorsal to the mesonephros (Fig. 224); by the end of the fifth day its anterior end has reached the level of the csecal appendages of the intestine, and on the eighth day its anterior end has reached its definitive position at the level of the vena cava inferior, near to the anterior end of the mesonephros (twenty-first definitive somite or twenty-fifth of the entire series; cf. Fig. 150).

It should be noted that the metanephric diverticulum is similar in its mode of origin to the so-called mesonephric ureters. It may in fact be regarded as the posterior member of this series, but it is separated from those that form the collecting tubules of the mesonephros by at least two somites in which no diverticula


THE URINOGEXITAL SYSTEM


385


of the mesonephros are formed (Fig. 219). During its growth forward a series of small diverticula arise from its wall and extend dorsally (Fig. 223); these branch secondarily in a generally dichot


,'-^i,< ■•'>"!■'■-■<- ■■■■---■: .




Af^Y.


^y^



Fig. 222. -Transverse section through the metanephros, mesonephros gonads and neighboring structures of an 11-day male chick, a. A. S., Abdominal air-.sac. Ao., Aorta B W Rndv wall r^^i n

duct. Mst., .Mesentery. M't'n., Metanephros. Sp., Spine of neural areh

W D^'woMandScrotr' '\t """.'^' "*'. J e.^., Vna ca"™ Meri*: vv . u., \^ oiman duct. Other abbreviations as before.


386


THE DEVELOPMENT OF THE CHICK



Fig. 223. — Profile reconstruction of the Wolffian duct and primordium of the metanephros of a chick embryo of 6 days and 8 hours. (After Schreiner.)

XXV to XXXIH, twentv-fifth to thirty-third somites. Al. N., Neck of allantois. CI., Cloaca. Int., Intestine. M's'n., Mesonephros. n. T., Nephroojenous tissue of the metanephros included within the dotted lines. W. D., Wolffian duct. Ur., Ureter.


THE URIXOGEXITAL SYSTEM 387

omoiis manner, and it is from them that the collecting tubules of the kidney arise; the posterior unbranched portion of the metanephric diverticulum represents the definitive ureter.

The following data concerning these branches should be noted:

(1) the first ones are formed from the posterior portion of the metanephric diverticulum, and the process progresses in an anterior direction. This is the reverse direction of the usual order of embryonic differentiation, but the reason for the order is the same, viz., that differentiation begins in the first formed parts.

(2) A posterior, smaller group of collecting tubules is separated at first by an unbranched portion of the ureter from an anterior larger group (Fig. 223). The unbranched region corresponds to the position of the umbilical arteries which cross here. (3) During the fifth and sixth days the terminal portion of the Wolffian duct common to both mesonephros and metanephros is gradually drawn into the cloaca, and thus the ureter obtains an opening into the cloaca independent of the Wolffian duct and posterior to it (Fig. 223).

The Nephrogenous Tissue of the Metanephros. The nephrogenous tissue of the thirty-first, thirty-second, and thirty-third somites is at first continuous with the mesonephros (Figs. 218 and 219), but on the fourth and fifth da3^s that portion situated immediately behind the mesonephros degenerates, thus leading to a complete separation of the most posterior portion situated in the neighborhood of the metanephric diverticulum. This constitutes the metanephrogenous tissue proper (inner zone). It is important to understand thoroughly its relations to the metanephric diverticulum. This is indicated in Fig. 219, which represents a graphic reconstruction of these parts in a duck embryo of 50 somites. It will be seen that the metanephrogenous tissue covers nearly the entire metanephric diverticulum; a transverse section (Fig. 224) shows that it lies on its median side. The outer dotted line (Fig. 219) gives the contour of a dense portion of mesenchyme related to the diverticulum and nephrogenous tissue proper. In section this forms a rather ill-defined area shading into the nephrogenous tissue on the one hand and into the surrounding mesenchyme on the other.

Fig. 224 shows the relations of the three constituent elements of the kidney at the end of the fifth day, as seen in a transverse section. The metanephric diverticulum lies on the median side


388


THE DEVELOPMENT OF THE CHICK


of the cardinal vein, and is in contact, on its median face, with the proper nephrogenous tissue (inner zone); the latter shades into the outer zone, the cells of which are arranged concentrically with reference to the other parts. The relations subsequently established may be summarized in a few Avords; the inner zone of tissue grows and branches pari passu with the growth and branching of the metanephric diverticulum, so that the termination of every collecting tubule is accompanied by a portion of



Fig. 224. — Transverse section through the

ureter and metanephrogenous tissue of a

5-day chick.

A. umb., Umbilical artery. Coel., Coelome.

M's't., Mesentery, n. t. i. z., Inner zone of the

nephrogenous tissue, n. t. o. z., Outer zone of

the nephrogenous tissue. Ur., Ureter. V. c.p.,

Posterior cardinal vein. W. D., Wolffian duct.

the inner zone, which is, however, always distinct from it. This conclusion is established by the fact that from the start the two elements, collecting tubules and inner zone, are distinct and may be traced continuously through every stage. The outer zone differentiates in advance of the two more essential constituents at all stages, and thus forms a rather thick investment

for them.

The formation of the secreting tubules from the inner zone


THE URIXOGEXITAL SYSTEM


389



Fig. 225. — Sections of the embryonic metanephros of the chick to show developing tubules. (After Schreiner.)

A. Nephric vesicle or primordium of secreting tubule (ur. t ) and collecting tubule (col. T.); 9 days and 4 hours.

B. Elongation of nephric vesicle; same embryo.

C. Indication of renal corpuscle at the distal end of the forming tubule.

D. The secreting tubule appears S-shaped.

E. Secreting tubule well formed; 9 davs and 21 hours.

F. Secreting tubule opening into collecting tubule; 11 days.


390 THE DEVELOPMENT OF THE CHICK

of the metanephrogenous tissue takes place in essentially the same manner as the formation of the mesonephric tubules. The first stages may be found in seven and eight-day chicks in the portion of the kidney behind the umbilical arteries. The inner zone tissue begins to arrange itself in the form of minute balls of cells in immediate contact with the secreting tubules; a small lumen then arises within the ball, transforming it into a thickwalled epithelial vesicle with radially arranged cells. The vesicle then elongates away from the collecting tubule and gradually takes on an S-shape. The distal end of the S becomes converted into a renal corpuscle as illustrated in Figure 225 and the proximal end fuses with the wall of the collecting tubule; an opening is then formed between the two.

On the eleventh day of incubation, secreting tubules are thus formed throughout the entire length of the kidney; but the histological structure does not yet give the effect of an actively secreting gland, although degeneration of the mesonephros has already begun. The full development of the nephric tubules in the chick has not been studied.

At all stages in its develojDment the kidney substance is separated from the mesonephros by a distinct layer of undifferentiated mesenchyme, which is, however, at certain times extremely thin. But there is no evidence that at any time elements of the mesonephros, e.g., undifferentiated nephrogenous tissue, extend up into the metanephric primordium which so closely overlies it (cf. Figs. 221 and 222).

The kidney is entirely retroperitoneal in its formation, and its primary capsule is established by differentiation of the periphery of the outer zone. This may be seen in process at eleven days (Fig. 222) : the primary capsule is definitely estal^lished on its median and lateral sides; but is defective dorsally and at the angle next the aorta. With the subsequent degeneration of the mesonephros, and projection of the kidney into the coelome, its ventral surface acquires a secondary peritoneal capsule.

III. The Organs of Reproduction

The gonads are laid down on the median surface, and the ducts on the lateral surface of the Wolffian body, which thus becomes converted into a urinogenital ridge. The composition of the urinogenital ridge is at first the same in all embryos, whether


THE URIXOGENITAL SYSTEM 391

destined to become male or female. It has three divisions: (1) the anterior or sexual division, containing the gonad, involves about the anterior half of the Wolffian body; (2) a non-sexual region of the Wolffian body occurs behind the gonad, and (3) behind the Wolffian body itself the urinogenital ridge contains only the Wolffian and Mullerian ducts. A transverse section through the anterior division shows the following relations (Fig. 221): on the mecUan surface the gonad, on the lateral surface near the dorsal angle of the body-cavity the Wolffian and Mullerian ducts, the latter external and dorsal to the former: between the gonad and ducts lie the tubules of the Wolffian body destined to degenerate for the most part.

There is an incUfferent stage of the reproductive system during which the sex of the embryo cannot be determined, either bv the structure of the gonad or the degree or mode of development of the ducts. In those embryos that become males the gonad develops into a testis, the Wolffian duct becomes the vas deferens, the tubules of the anterior part of the Wolffian body become the epididymis, those of the non-sexual part degenerate, leaving a rudiment known as the paradidymis, and the Mullerian duct becomes rudimentary or disappears. In embryos that become females, the gonad develops into an ovary; the Wolffian duct disappears or becomes rudimentary, the Mullerian duct develops into the oviduct on the left side and disappears on the right side, and the tubules of the Wolffian body degenerate, excepting that functionless homologues of the epididymis and paradidymis persist, known as the epoophoron and paroophoron respectively.

It is not correct to state, as is sometimes done, that the embryo is primitively hermaphrodite, for, though the ducts characteristic of both sexes develop equally in all embryos, the primitive gonad is, typically, only indifferent. Nevertheless, if the gonad be physiologically as well as morphologically indifferent in its primitive condition, the possibility of an hermaphrodite development is given. The primitive embryonic conditions appear to furnish a basis for any degree of development of the organs of both sexes.

Development of Ovary and Testis. Indifferent Period. The reproductive cells of ovary and testis alike arise from a strip of peritoneal epithelium, known as the germinal epithelium, which is differentiated on the fourth day by its greater thickness


392 THE DEVELOPMENT OF THE CHICK

from the adjacent peritoneum (Fig. 217). The germinal epithelium lies between the base of the mesentery and the mesonephros at first, but as the latter grows and projects into the body-cavity the germinal epithelium is drawn on to its median surface. It is difficult to determine its antero-posterior extent in early stages; it begins near the point of origin of the omphalomesenteric arteries, and its posterior termination is indefinite, but it certainly extends over seven or eight somites.

Two kinds of cells are found in the germinal epithelium, viz., the ordinary peritoneal cells and the primordial germ-cells. The latter are typically round, and several times as large as the peritoneal cells (Figs. 226 and 227); the cytoplasm is clear but contains persistent yolk granules and a large attraction sphere, and the nucleus contains one or two nucleoli; they are sharply distinguishable from the peritoneal cells, and they may be traced through a continuous series of later developmental stages into the ova and spermatozoa. The origin of these primordial germ-cells is therefore a matter of considerable interest.

Two views have been held: (1) that they are derived from the peritoneal cells, and (2) that they have an independent history antecedent to the differentiation of a germinal epithelium, representing in fact undifferentiated embryonic cells that reach the germinal epithelium by migration from their original source. The former view was due to Waldeyer, and was supported by observations of cells intermediate in structure between the primordial germ-cells and cells of the peritoneum (e.g. by Semon). These observations have, however, been shown to be erroneous. The second view has been demonstrated for a considerable number of vertebrates; and quite recently Swift has shown that the primordial germ-cells of the chick arise from the germ-wall at the anterior margin of the pellucid area in a late stage of the primitive streak; that they later enter the blood stream and are carried into the embryo; some, which reach various inappropriate positions, degenerate; but others leaving the blood near the base of the mesentery reach the germinal epithelium by migration. The independent and early origin of germ-cells has an obvious bearing on the theory of the continuity of the germ-plasm of Weismann.


THE URINOGENITAL SYSTEM


393


Two other epithelial constituents enter into the composition of the indifferent gonad, viz.: the rete tissue or cords of the urinogenital union, and the sexual cords. These lie between the germinal epithelium and the glomeruli of the Wolffian body. Between these elements is a sparse mesenchyme continuous with the surrounding mesenchyme, constituting the stroma of the gonad.


.*,^


V


ty.b





• V^


^V^.-_





m


w -*■•« ' * '


'A~s t.


Fig. 226. — Cross-section through the genital primordium of Limosa segocephala. (After Hoffmann, from Fehx and Biihler.)

The stage is similar to that of a chick embryo of 4| days.

Germ., Germinal epithelium. Mst., Mesentery. S. C., Rete cords. v., Posterior cardinal vein. W. D., Wolffian duct.


Some primordial germ-cells occur in the stroma, though most are in the germinal epithelium.

The rete cords appear within the gonad on the fifth day; they are solid cords of epithelial cells that fill up the interior


394 THE DEVELOPMENT OF THE CHICK

of the gonad and cause it to protrude from the surface of the Wolffian body (Fig. 226); the cords extend from the germinal epithelium towards the hilum of the gonad (represented at this time by the broad surface opposed to the Wolffian body), and into the Wolffian body where they enter into close connection with the renal corpuscles. In the Wolffian body and intermediate zone they are very irregular in their course and connected by numerous anastomoses, corresponding to the rete region of the future testis. Strands of these cells pass dorsally, and, according to some authors, form the cortical cords of the suprarenal capsules (Fig. 226).

The following views of the origin of the rete cords in birds have been held: (1) That they arise as outgrowths of the capsules of renal corpuscles (Hoffmann, Semon) and the neck of the Wolffian tubules also (Semon); (2) that they are ingrowths of the germinal epithelium (Janosik); (3) that they differentiate from the stroma (Prenant, Firket). The subject is a somewhat difficult and complicated one, but the view that the rete cords arise as outgrowths of the capsules of renal corpuscles brings the birds into line, in this respect, with the reptiles and amphibia. Hoffmann's observation that the rete cords lie at first on the lateral side of the blood-vessels intervening between the germinal epithelium and the Wolffian body, and that the cells of the cords are directly continuous with those of the capsules, should be conclusive.

The sexual cords arise as proliferations of the germinal epithelium which appear as buds projecting into the stroma (Fig. 227). They are definitely limited in time of origin between the middle of the fifth and sixth days of incubation (Swift). They carry with them numerous primordial germ-cells from the germinal epithelium. About the end of the sixth day all free themselves from the germinal epithelium, and a layer of stroma begins to separate them sharply from the latter. They are destined to form the seminiferous tubules in the male, and the so-called medullary cords in the female.

Sexual Differentiation. The period of morphological indifference of the gonad is relatively long and the actual sexual differentiation appears slowly. It manifests itself (1) in differences in the behavior of the germinal epithelium; (2) of the sexual cords;


THE URINOGENITAL SYSTEM


395


(3) larger size of the left ovary and ultimate disappearance of the right one; (4) behavior of the stroma, particularly the albuginea. The sex of the embryo can first be definitely determined about the 156th hour, by the relative sizes of the two gonads, by the behavior of the germinal epithelium and by the presence of a larger


K,'-^




germ. ep.


pro.


m.


y^^/.




4



coelom



.fSf







Fig. 227. — Portion of a transverse section through an ovary of a 6^ day chick embryo (after Swift), germ, ep., germinal epitheHum. m. c, sexual cord. pr. o., primordial germ-cells.

number of primordial germ-cells in the germinal epithelium of

the female. (Swift.)

As already stated, the sexual cords form the seminiferous tubules of the testis; they are made up of two kinds of cells, viz.: the primordial germ-cells and the ordinary peritoneal cells derived from the germinal epithelium. After the seventh day they constitute most of the bulk of the testis, and the rete cords are pressed towards the hilum by the sexual cords which radiate in that direc


396


THE DEVELOPIMENT OF THE CHICK


tion. The sexual cords now begin to branch and anastomose, and soon form a reticulmn with mesenchyme in the meshes. About the thirteenth day the primordial germ-cells, which have been inactive, begin to divide, and a rapid increase in numbers ensues.


Intc. sir.



> -*=




m^f




'^:y/:


•%


vSJ*;*


?^:


.?*'


?,i'




Fig. 228. — Portion of a transverse section through the right testis of a 20 day chick embryo. The section shows a seminiferous cord in which a lumen is beginning to develop. Note the position and polarization of the spermatogonia (after Swift). Int. c, interstitial cells. L., beginning of lumen. M. C, Mitochondrial granules within a spermatogonium, p. c, supporting cells, derivatives of peritoneal cells of the sexual cords, s. c, seminiferous cord, sp., spermatogonia, str., stroma.

The sexual cords are solid up to about the twentieth day of incubation; a lumen then begins to appear and they become transformed into tubules (Fig. 228). The primordial germ-cells form the spermatogonia, and the peritoneal cells form the supporting cells of the seminiferous tubules (Swift).

After the sixth day the germinal epithelium of the testis rapidly retrogresses and becomes reduced to a thin peritoneal


THE URIXOGENITAL SYSTEM 397

endothelium. The stroma of the primitive testis remains scanty up to the eleventh day. It then increases rapidly between the sexual cords and also forms a layer between germinal epithelium and seminiferous tubules, which becomes the albuginea. Interstitial cells appear in the stroma of the testis about the thirteenth day and increase so rapidly as to form an immense amount by the twentieth day (Swift).

As the testis increases in size it projects more from the surface of the Wolffian body, and folds arise above and below it as well as in front and behind, that progressively narrow the surface of apposition, which in this way becomes gradually reduced to form the hilum of the testis, through which the rete cords pass to the neighboring renal corpuscles (cf. Figs. 221 and

222).

As the testis is attached to the anterior portion of the Wolffian body, the latter may be divided in two portions, an anterior sexual and a posterior non-sexual portion. In the latter part of the period of incubation the non-sexual portion undergoes absorption while the anterior portion becomes converted into the

epididymis.

The irregularly anastomosing rete cords in the region of the hilum are united to the neighboring renal corpuscles by the original strands and these form the vasa efferentia. In order to complete the urinogenital union it is necessary that the rete cords unite with the seminiferous tubules. The exact manner in which this takes place has not been worked out for the chick; but there is no doubt that this union does take place so that the seminiferous tubules connect by way of the rete with the mesonephric tubules and thus with the Wolffian duct.

As regards the formation of the epididymis: the renal corpuscles of the Wolffian tubules concerned diminish in size, the glomerulus disappears and the cells of the capsule become cylindrical. These changes progress from the lateral side of the Wolffian body towards the testis; that is to say, the more lateral corpuscles are first affected. A rudiment of the non-sexual part of the Wolffian body persists in the . mesorchium of the male, between testis and kidney. It is known as the paradidymis.

The development of the ovary in the chick has been studied in recent years by Firket and by Swift.

The right ovary never undergoes much development after


398


THE DEVELOPMENT OF THE CHICK


the indifferent stage; it is destined to retrogress, and finally it disappears.

In the indifferent gonad the sexual cords are formed in the same way whether the organ is to become ovary or testis; but, whereas in the case of the testis these cords are destined to form the functional seminiferous tubules, in the case of the ovary they form only the cords of the medulla. The cortex of the ovary which includes the functional follicles develops from a second



Fig. 229. — Cross-section of the ovary of a young embryo of Numenius arcuatus. (After Hoffmann.) bl. v., Blood-vessel, germ. Ep., Germinal epithelium, r., rete ovarii. s. c, Sexual cord.

proHferation of the germinal epithelium. The sexual cords cease to grow, and become converted into tubes with a wide lumen, and low epithehum; shortly after hatching they entirely disappear.

The characteristic feature of the development of the ovary is a second period of intensive growth of the germinal epithelium accompanied by a rapid increase of the primordial germ-cells contained in it. This goes on very rapidly during the eighth to the eleventh days of incubation. The inner surface of the germinal epithelium, or ovigerous layer of the ovary, begins to form


THE URIXOGEXITAL SYSTEM


399


low irregular projections into the stroma, or the latter begins to penetrate the ovigerous layer at irregular distances so as to produce elevations. This condition is well illustrated in Fig. 229.

In the course of development the ovigerous layer continually increases in thickness, and the projections into the stroma form veritable cords of ovigerous tissue, which correspond to the


i^s^^iS:


^^





Fig. 230. — Cross-section of the ovary of a fledgling of Numenius arcuatus 3-4 days old. The germinal epithelium is below. (After Hoffmann.) s. c, Sexual cords.

cords of Pfltiger in the mammalian ovary. The cords carry the primitive ova with them. The surface of the ovary also begins to become lobulated by the extension of the stroma trabeculae. Successive stages in the growth and differentiation of the primitive ova occur from the surface towards the inner ends of the ovigerous strands. Fig. 230 represents a section through


400 THE DEVELOPIMENT OF THE CHICK

the ovary of a fledgling of Numenius arcuatus three or four days old. The germinal epithelium covers the surface and is continuous with the ovigerous strands projecting far into the stroma. The strands are broken up in the stroma into nests of cells; next the germinal epithelium are found characteristic primitive ova, but in deeper situations the primitive ova are larger and each is accompanied by a group of epithelial cells, which are distinctly differentiated as granulosa cells of young follicles in the deepest. Thus the young follicles arise by separation of nests of cells from the ovigerous strands within the stroma; each nest includes a young ovocyte and a group of epithelial cells which arrange themselves in a single layer of cuboidal cells around the ovocyte. On each side of the free border of the ovary the embryonic state persists, and it is not known whether this condition is maintained permanently, as in some reptiles, or not.

The atrophy of the Wolffian body is much more complete in the female than in the male; no part of it remains in a functional condition, but the part corresponding to the epididymis of the male remains as a rudiment, known as the epoophoron. It has almost the same structure in young females as in young males, but the rete cords uniting it with the ovary do not become tubular. A rudiment of the non-sexual part of the Wolffian body is also found in the hen between ovary and Iddney in the lateral part of the mesovarium; it has been named the paroophoron.

Development of the Genital Ducts. The Wolffian Duct. The origin and connections of the Wolffian ducts have been already sufficiently described. In the male they are connected with the seminiferous tubules by way of the epididymis, vasa efferentia, and rete, and function as vasa deferentia exclusively, after degeneration of the mesonephros. Subsequently they become somewhat convoluted, acquire muscular walls and a slight terminal dilatation. The details of these changes are not described in the literature. In the female the Wolffian duct degenerates; at what time is not stated in the literature, but presumably along with the Wolffian body.

The Mullerian Duct. The Miillerian duct, or oviduct, is laid down symmetrically on both sides in both male and female embryos; subsequently both right and left ]\Iiillerian ducts degenerate in the male; in the female the right duct degenerates, the


THE URIXOGEXITAL SYSTEM 401

left only remaining as the functional oviduct. We have now to consider, therefore, (1) the origin of the ducts during the indifferent stage, and (2) their subsequent history in the male and in the female.

The origin of the IMlillerian duct is preceded by the formation of a strip of thickened peritoneum on the lateral and superior face of the Wolffian body extending all the way to the cloaca (cf. Fig. 220). This strip, which may be called the tubal ridge, appears first at the anterior end of the Wolffian body on the fourth da}", and rapidly differentiates backwards; it lies immediately external to the Wolffian duct. The anterior part of the Miillerian duct arises as a groove-like invagination of the tubal ridge at the cephalic end of the Wolffian body immediately behind the external glomeruli of the pronephros. The hps of this groove then approach and fuse on the fifth day, so as to form a tube which soon separates from the ridge. This process, however, takes place in such a way as to leave the anterior end of the tube open and this constitutes the coelomic aperture of the oviduct, or ostium tuh(£ abdominale. Moreover, the closure of the groove does not take place uniformly, and one or two openings into the Miillerian duct usually occur near the ostium on the fifth clay. Typically, however, these soon close up, though persistence of one of them may lead, as a rather rare abnormality, to the occurrence of two ostia in the adult. There is no ground for the view (see Balfour and Sedgwick) that the two or three openings into the anterior end of the Miillerian duct correspond to nephrostomes of the pronephros; they are situated too far posteriorly and laterally to bear such an interpretation.

The anterior part of the Miillerian duct is thus formed by folding from the epithelium of the tubal ridge; it constitutes a short epithelial tube situated between the Wolffian duct and the tubal ridge, ending blindly behind. The part thus formed is relatively short; the major portion is formed by elongation of the anterior part, which slowly grows backwards between the Wolffian duct and the tubal ridge, reaching the cloaca on the seventh day. The growing point is solid and appears to act like a wedge separating the Wolffian duct and the tubal ridge, being thus closely pressed against both, but apparently without receiving cells from either. Balfour's view, that it grows by splitting off from the Wolffian duct or at the expense of cells contributed by the latter,


402 THE DEVELOPAiEXT OF THE CHICK

has not been supported by subsequent investigators. A short distance in front of the growing point the Mullerian duct receives a kuiien, and mesenchyme presses in from above and below, and forms a tunic of concentrically arranged cells around it

(Fig. 221).

The ]Mullerian duct thus begins to project above the surface of the Wolffian body, and, as it does so, the thickened epithelium of the tubal ridge becomes flat and similar to the adjacent peritoneum; whether it is used up in the formation of the mesenchymatous tunic of the epithelial Mullerian duct is not known. Up to this time the development is similar in both sexes and on both sides of the body.

In the male development of these ducts ceases on the eighth day; retrogression begins immediately and is completed, or at any rate far advanced, on the eleventh day. In this process the epithelial wall disappears first, and its place is taken by cells of mesenchymatous appearance, though it is not known that transformation of one kind into the other takes place. Retrogression begins posteriorly and proceeds in the direction of the head; the ostium is the last to disappear. The mesenchymatous tunic shares in the process, so that the ridge is no longer found (see Fig. 222). In the male the IMullerian ducts never open into

the cloaca.

In the female the development of the right Mullerian duct ceases after the eighth day, and it soon begins to degenerate. Its lumen disappears and it becomes relatively shorter, so that its anterior end appears to slip back along the Wolffian body. On the fifteenth day slight traces remain along its former course and a small cavity in the region of the cloaca. It never obtains an opening into the cloaca (Gasser).

With the degeneration of the anterior end of the Wolffian body the ostium tubse abdominale comes to be attached by a Ugament to the body-wall (Fig. 231); farther back the ligamentous attachment is to the Wolffian body.

The fimbriae begin to develop on the eighth day on both sides in both sexes. It is only in the left oviduct of the female, however, that development proceeds farther, and differentiation into ostium, glandular part, and shell gland takes place. This appears distinctly about the twelfth day. The lower end expands to form the primordium of the shell


THE URIXOGEXITAL SYSTEM


403


gland at this time, but does not open into the cloaca. Indeed, the opening is not established until after the hen is six months old (Gasser.)


Aom


M'cj2


pl.C.r


/iec.p/j.e/iii'


o.r.a




Vcd.l.


Aar.v.c


Fig. 231. — Photograph of a cross-section of an embryo of 8 clays through the

ostia tubae abdominaha.

a. A. S., Xeck of abdominal air-sac. O. T. a., Ostium tubae abdominale. M's't.ac, Accessory mesentery, pi. C. r., 1., Right and left pleural cavities. Rec. pn. ent. r., Right pneumato-enteric recess. V. c. a. 1., Left anterior vena cava. R., rib. Other abbreviations as before.


IV. The Suprarenal Capsules

The suprarenals of the hen are situated medial to the anterior lobe of the kidney, in the neighborhood of the gonad and vena cava inferior. They have a length of about 8-10 mm. The substance consists of two kinds of cords of cells, known respectively as cortical and medullary cords, irregularly intermingled: the so-called cortical cords make up the bulk of the substance, and the medullary cords occur in the meshes of the cortical cords.


404 THE DEVELOPMENT OF THE CHICK

The terminology does not, therefore, describe well the topographical arrangement of the components; it was derived from the condition found in many mammals, the cortical cords of the birds corresponding to the cortical substance, and the medullary cords to the medullary substance of mammals. The medullary cords are often called phseochrome or chromaffin tissue on account of the specific reaction of the constituent cells to chromic acid, and their supposed genetic relation to tissue of similar composition and reaction found in the carotid glands and other organs associated with the sympathetic system.

The embryonic history has been the subject of numerous investigations, and has proved a particularly difficult topic, if we are to judge from the variety of views propounded. Thus for instance it has been maintained at various times: (1) that cortical and medullary cords have a common origin from the mesenchyme; (2) that they have a common origin from the peritoneal epithehum; (3) that the origin of the cortical and medullary cords is absolutely distinct, the former being derived from the sexual cords by way of the capsules of the renal corpuscles and the latter from the sympathetic ganglia; (4) that their origin is distinct, but that the cortical cords are derived from ingrowths of the peritoneum, and the medullary cords from sympathetic ganglia. The first view may be said now to be definitely abandoned, and no one has definitely advocated a common epithehal origin since Janosik (1883). Thus it may be regarded as well estabUshed that the two components have diverse origins, and it seems to the writer that the fourth view above is the best supported. (See Poll and Soulie.) The comparative embryological investigations strongly support this view.

Origin of the Cortical Cords. According to Soulie, the cortical cords arise as proliferations of a special suprarenal zone of the peritoneum adjacent to the anterior and dorsal part of the germinal epithehum. This zone is distinguishable early on the fourth day, and begins about half a millimeter behind the glomeruH of the pronephros, extending about a millimeter in a caudal direction. Proliferations of the peritoneal epithelium are formed in this zone, and soon become detached as groups of epithelial cells lying in the mesenchyme between the anterior end of the Wolffian body and the aorta. Such proliferation con


THE URINOGEXITAL SYSTEM 405

tinues up to about the one hundredth hour or a httle later, and a second stage in the development of the cortical cords then begins: The cords grow rapidly and fill the space on the mediodorsal aspect of the AVolffian body, and then come secondarily into relation with the renal corpuscles of the latter and the sexual cords.

According to Semon and Hoffmann the relation thus established is a primary one, that is to say, that the cortical cords arise from the same outgrowths of the capsules of the renal corpuscles that furnish the sexual cords. Rabl agrees essentially with Soulie, and it seems probable that Semon and Hoffmann have overlooked the first stages in the origin of the cortical cords of the suprarenal corpuscles.

During the fifth, sixth, and seventh days there is a very rapid increase of the cortical cords accompanied by a definite circumscription of the organ from the surrounding mesenchyme; however, no capsule is formed yet. The topography of the organ on the eighth day is shown in Figs. 150 and 182. Whereas during the fourth, fifth, and sixth days the arrangement of the cortical cells is in masses rather than in cords, on the eighth day the cords are well developed, in form cylindrical with radiating cells, but no central lumen. The organ has become vascular, and the vessels have the form of sinusoids, i.e., they are moulded on the surface of the cords with no intervening mesenchyme.

Origin of the Medullary Cords. The medullary cords take their origin unquestionably from cells of the sympathetic nervous system. During the growth of the latter towards the mesentery, groups of sympathetic cells are early established on or near the dorso-median surface of the cortical cords (Fig. 226). The ingrowth of the sympathetic medullary cords does not, however, begin until about the eighth day. At this time there is a large sympathetic ganglionic mass on the dorso-median surface of the anterior end of the suprarenal, and strands of cells characterized sharply by their large vesicular nuclei and granular contents can be traced from the ganglion into the superficial part of the suprarenal. These cells are precisely like the specific cells of the ganglion, perhaps a little smaller, and without axones. On the eleventh day these strands have penetrated through a full third of the thickness of the suprarenal, and are still sharply characterized, on the one hand by their resemblance to the


406 THE DEVELOPMENT OF THE CHICK

sympathetic ganglion cells, and on the other by their clear differentiation from the cells of the cortical cords. These occupy the relations characteristic of the differentiated medullary cords, and there can be httle doubt that they develop into them.


CHAPTER XIV THE SKELETON

I. General

From an embryological point of view, tlie bones of the body, their associated cartilages, the ligaments that unite them together in various ways, and the joints should be considered together, as they have a common origin from certain aggregations of mesenchyme. The main source of the latter is the series of sclerotomes, but most of the bones of the skull are derived from the unsegmented cephalic mesenchyme.

Most of the bones of the body pass through three stages in their embryonic development: (1) a membranous or prechondral stage, (2) a cartilaginous stage, (3) the stage of ossification. Such bones are known as cartilage bones, for the reason that they are preformed in cartilage. Many (see p. 433 for list) of the bones of the skull, the clavicles and the uncinate processes of the ribs do not pass through the stage of cartilage, but ossification takes place directly in the membrane; these are known as membrane or covering bones. The ontogenetic stages of bone formation parallel the phylogenetic stages, membrane preceding cartilage, and the latter preceding bone in the taxonomic series. Thus, in Amphioxus, the skeleton (excluding the notochord) is membranous; in the lamprey eel it is partly membranous and partly cartilaginous; in the selachia it is mainly cartilaginous; in higher forms bone replaces cartilage to a greater or less degree. The comparative study of membrane bones indicates that they were primitively of dermal origin, and only secondarily grafted on to the underlying cartilage to strengthen it. Thus the cartilage bones belong to an older category than the membrane bones.

The so-called membranous or prechondral stage of the skeleton is characterized simply by condensation of the mesenchyme. Such condensations arise at various times and places described

407


408 THE DEVELOPMENT OF THE CHICK

beyond, and they often represent the primordia of several future bony elements. In such an area the cells are more closely aggregated, the intercellular spaces are therefore smaller, and the area stains more deeply than the surrounding mesenchyme. There are, of course, stages of condensation in each case, from the first vague and undefined areas shading off into the indifferent mesenchyme, up to the time of cartilage or bone formation, when the area is usually well defined. In most of the bones, however, the process is not uniform in all parts; the growing extremities may be in a membranous condition while cartilage formation is found in intermediate locations and ossification has begun in the original center of formation; so that all three stages may be found in the primordium of a single bone {e.g., scapula). Usually, however, the entire element is converted into cartilage before ossification begins.

The formation of cartilage (chondrification) is brought about by the secretion of a homogeneous matrix of a quite special character, which accumulates in the intercellular spaces, and thus gradually separates the cells; and the latter become enclosed in separate cavities of the matrix; when they multiply, new deposits of matrix form between the daughter cells and separate them. As the original membranous primordium becomes converted into cartilage, the superficial cells flatten over the surface of the cartilage and form a membrane, the perichondrium, which becomes the periosteum when ossification takes place.

The process of ossification in the long bones involves the following stages in the chick:

(1) Formation of Perichondral Bone. The perichondrium deposits a layer of bone on the surface of the cartilage near its center, thus forming a bony ring, which gradually lengthens into a hollow cylinder by extending towards the ends of the cartilage. This stage is well illustrated in Fig. 231 A and in the long bones of Fig. 242; the bones of the wing and leg furnish particularly good examples; the perichondral bone is naturally thickest in the center of the shaft and thins towards the extremity of the

cartilages.

(2) Absorption of Cartilage. The matrix softens in the center of the shaft and becomes mucous, thus liberating the cartilage cells and transforming the cartilage into the fundamental tissue of the bone marrow. This begins about the tenth


THE SKELETON


409


day in the femur of the chick. The process extends towards the ends, and faster at the periphery of the cartilage {i.e., next to the perichondral bone) than in the center. In this way there remain two terminal, cone-shaped cartilages, and the ends of the cones project into the marrow cavity (Fig. 231 A).

(3) Calcification of Cartilage. Salts of lime are deposited in the matrix of the cartilage at

the ends of the marrow cavity; such cartilage is then removed by osteoclasts, large multinucleated cells, of vascular endothelial origin, according to Brachet (seventeenth or eighteenth day of incubation).

(4) Endochondral Ossification. Osteoblasts within the marrow cavity deposit bone on the surface of the rays of calcified cartilage that remain between the places eaten out by osteoclasts, and on the irmer surface of the perichondral bone.

These processes gradually extend towards the ends of the bone, and there is never any independent epiphysial center of ossification in long bones of birds, as there is in mammals. The ends of the bones remain cartilaginous and provide for growth in length. Growth in diameter of the bones takes place from the periosteum, and is accompanied by enlargement of the marrow cavity, owing to simultaneous absorption of the bone from within. It is thus obvious that all of the endochondral bone is removed from the shaft in course of time; some remains in the spongy ends.

The details of the process of ossification will not be described here, and it only remains to emphasize a few points. At a stage shortly after the beginning of absorption of the cartilage in the



Fig. 231 A. — Longitudinal section of the femur of a chick of 196 hours' incubation; semi-diagrammatic. (After Brachet.)

art. Cart., Articular cartilage. C. C, Calcified cartilage, end. B., Endochondral bone. M., Marrow cavity. P'ch., Perichondrium. P'os., Periosteum, p'os. B., Periosteal bone. Z. Gr., Zone of growth. Z. Pr., Zone of proliferation. Z. R., Zone of resorption.


410 THE DEVELOPMENT OF THE CHICK

center of the shaft, the perichondral bone is invaded by capillary vessels and connective tissue that break through into the cavity formed by absorption; it is supposed by many that osteoblasts from the periosteum penetrate at the same time. The marrow of birds is derived, according to the best accounts, from the original cartilage cells, which form the fundamental substance, together with the intrusive blood-vessels and mesenchyme. The endochondral osteoblasts are believed by some to be of endochondral origin (i.e., derived from cartilage cells), by others of periosteal origin. For birds, the former view seems to be the best supported.

In birds, calcification does not precede absorption of the cartilage, as it does in mammals, until the greater part of the marrow cavity is formed. The cones of cartilage, referred to above, that are continuous with the articular cartilages, are absorbed about ten days after hatching.

On the whole, perichondral ossification plays a more extensive role in birds than in mammals. The endochondral bone formation begins relatively much later and is less extensive. The bodies of the vertebrae, which ossify almost exclusively in an endochondral fashion, form the main exception to this rule.

Ossification in membrane proceeds from bony spicules deposited between the cells in the formative center of any given membrane bone. It spreads out from the center, the bony spicules forming a network of extreme delicacy and beauty. After a certain stage, the membrane bounding the surface becomes a periosteum which deposits bone in dense layers. Thus a membrane bone consists of superficial layers of dense bone, enclosing a spongy plate that represents the primitive bone before the establishment of the periosteum.

The formation of bones proceeds from definite centers in all three stages of their formation; thus we have centers of membrane formation, centers of chondrification and centers of ossification. Membranous centers expand by peripheral growth, cartilage centers expand by the extension of cartilage formation in the membrane from the original center of chondrification, and bony centers expand in the original cartilage or membrane. Several centers of chondrification may arise in a single primitive membranous center; for instance, in the membranous stage, the skeleton of the fore-limb and pectoral girdle is absolutely con


THE SKELETON 411

tinuoiis; cartilage centers then arise separately in different parts for each of the bones: similarly for the hind-limbs and pelvic girdle, etc. Separate centers of ossification may likewise appear in a continuous embryonic cartilage, as for instance, in the base of the skull or in the cartilaginous coraco-scapula, or ischioilium. Such centers may become separate bones or they may subsequently fuse together. In the latter case, they may represent bones that were phylogenetically perfectly distinct elements, as for instance, the prootic, epiotic, and opisthotic centers in the cartilaginous otic capsule; or they may be of purely functional significance, as for instance, the separate ossifications in the sternum of birds, or the epiphysial and diaphysial ossifications of the long bones of mammals. It is usually possible on the basis of comparative anatomy to distinguish these two categories of ossification centers.

Phylogenetic reduction of the skeleton is also usually indicated in some manner in the embryonic history. Where elements have completely disappeared in the ph3dogenic history, as for instance, the missing digits of birds, they often appear as membrane formations in the embrvo, which then fade out without reaching the stage of cartilage; if the latter stage is reached the element usually fuses with some other and is therefore not really missing, e.g., elements of the carpus and tarsus of birds (though not all). But the ontogenetic reduction may go so far that the missing elements are never distinguishable at any stage of the embryonic history; thus, though the missing digits of birds are indicated in the membranous stage, their component phalanges are not indicated at all.

II. The Vertebral Column

The primordia of the vertebral column are the notochord and sclerotomes. The former is the primitive axial support of the body, both ontogenetically and phylogenetically. In both components, notochord and sclerotomes, we may recognize a cephalic and trunk portion. The notochord, as we have seen, extends far into the head, and the sclerotomes of the first four somites contribute to the formation of the occipital portion of the skull. The cephalic parts are dealt with in the development of the skull. The history of the notochord and sclerotomes will be considered together, but we may note in advance that the


412 THE DEVELOPMENT OF THE CHICK

notochord is destined to be completely replaced by the bodies of the vertebrae, derived from the sclerotomes.

The Sclerotomes and Vertebral Segmentation. The vertebral segmentation does not agree with the primitive divisions of the somites, but alternates with it; or in other words, the centers of the vertebrae do not coincide with the centers of the original somites, but with the intersomitic septa in which the segmental arteries run. Thus each myotome extends over half of two vertebral segments, and the spinal ganglia and nerves tend to alternate with the vertebrae. It therefore happens that each myotome exerts traction on two vertebrae, obviously an advantageous arrangement, and the spinal nerves lie opposite the intervertebral foramina.

This arrangement is brought about by the development of each vertebra from the caudal half of one sclerotome and the cephalic half of the sclerotome immediately behind; parts of two somites enter into the composition of each vertebra, as is very obvious at an early stage: Fig. 232 represents a section through the base of the tail of a chick embryo of ninety-six hours; it is approximately frontal, but is inclined ventro-dorsally from behind forwards. The original somites are indicated by the myotomes and the segmental arteries. In the region of the notochord one can plainly distinguish three parts to each sclerotome, viz., (1) a narrow, median, or perichordal part abutting on the notochord, in which no cUvisions occur either within or between somites; (2) a caudal lateral cUvision distinguished by the denser aggregation of the cells from (3) the cephalic division. Between the caudal and cephalic cUvisions of the sclerotome is a fissure (intervertebral fissure) which marks the boundary of the future vertebrae. Each vertebra in fact arises from the caudal component of one sclerotome and the cephalic component of the sclerotome immediately behind. Between adjacent sclerotomes is the intersomitic septum containing the segmental artery. If one follows these conditions back into successively earlier stages, one finds that the intervertebral fissure arises from the primitive somitic cavity, and that the distinction between caudal and cephalic divisions of the sclerotome is marked continuously from a very early stage by the presence of the intervertebral fissure and the greater density of the caudal division, i.e., the cephalic component of each definitive vertebra.


THE SKELETOX


413




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Fig. 232.— Frontal section through the base of the tail of a chick embryo of 96 hours. The anterior end of the section (above in the figure) is at a higher plane than the posterior end. caud. Scl., Caudal division of the sclerotome, ceph Scl Cephalic division of the sclerotome. Derm., Dermatome. Ep., Epidermis. Gn., Ganglion, int's. F., Intersomitic fissure int'v F Intervertebral fissure. My., Mvotome. N'ch., Notochord Nt' Neural tube, per'ch. Sh., Perichordal sheath, s. A., Segmental artery.


414 THE DEVELOPMENT OF THE CHICK

Now, if one follows these components as they appear at successively higher levels in such a frontal section as Fig. 232, one finds that the perichordal layer disappears in the region of the neural tube, and that the spinal ganglia appear in the cephalic division of the sclerotome, and almost completely replace it. Thus the caudal division of the sclerotome is more extensive, as well as denser, than the cephalic division.

In transverse sections one finds that the sclerotomic mesenchyme spreads towards the middle line and tends to fill all the interspaces between the notochord and neural tube, on the one hand, and the myotomes on the other. But there is no time at which the sclerotome tissue of successive somites forms a continuous unsegmented mass in which the vertebral segmentation appears secondarily, as maintained by Froriep, except in the thin perichordal layer; on the contrary, successive sclerotomes and vertebral components may be continuously distinguished, except in the perichordal layer; and the fusion of caudal and cephalic sclerotome halves to form single vertebrae may be continuously followed. Thus, although the segmentation of the vertebrae is with reference to the myotomes and ganglia, it is dependent upon separation of original sclerotome halves, and not secondarily produced in a continuous mass.

Summarizing the conditions at ninety-six hours, we may say that the vertebrae are represented by a continuous perichordal layer of rather loose mesenchvme and two mesenchvmatous arches in each segment, that ascend from the perichordal layer to the sides of the neural tube; in each segment the upper part of the cephalic sclerotomic arch is occupied almost completely by the spinal ganglion, but the caudal arch ascends higher, though not to the dorsal edge of the neural tube. The cranial and caudal arches of any segment represent halves of contiguous, not of the same, definitive vertebra.

Membranous Stage of the Vertebrae. In the following or membranous stage, the definitive segmentation of the vertebrae is established, and the principal parts are laid down in the membrane. These processes are essentially the same in all the vertebrae, and the order of development is in the usual anteroposterior direction. As regards the establishment of the vertebral segments: Figs. 233 and 234 represent frontal sections through the same vertebral primordia at different levels from


THE SKELETON


415


the thoracic region of a five-day chick. The notochord is slightly constricted intervertebrally, and the position of the intersegmental artery, of the myotomes and nerves, shows that each vertebral segment is made up of two components representing succeeding sclerotomes. In the region of the neural arches (Fig. 234) the line of union of cranial and caudal vertebral components is indicated by a slight external indentation at the place of union, and by the arrangement of the nuclei on each side of the plane of union.


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Fig. 233. — Frontal section through the notochord and pri mordia of two vertebrae of a 5-day chick; thoracic region.

Note intervertebral constrictions of the notochord. The

anterior end of the section is above.

N., Spinal nerve. Symp., Part of sympathetic cord. v. C, Region of pleurocentrum, in which the formation of cartilage


has hegun.


Other abbreviations as in Fig. 232.


The parts of the vertebrae formed in the membranous stage are as follows: (1) The vertebral body is formed by tissue of both vertebral components that grows around the perichordal sheath; (2) a membranous process (neural arch) extends from the vertebral body dorsally at the sides of the neural canal; but the right and left arches do not yet unite dorsally; (3) a lateral or costal process extends out laterally and caudally (Fig. 233) from the vertebral body between the successive myotomes.

The union of the right and left cephalic vertebral components


416


THE DEVELOPMENT OF THE CHICK


(caudal sclerotome halves) beneath the notochorcl is known as the subnotochordal bar (Froriep). It forms earlier than the remainder of the body of the vertebra and during the membranous stage is thicker, thus forming a ventral projection at the cephalic end of the vertebral body that is very conspicuous (Fig. 235).


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Fig. 234. — Frontal section including the same vertebral primordia as Fig. 233, at a higher level through the neural arches, a. C, Anterior commissure of the spinal cord. v. R., Ventral root of spinal nerve. Other abbreviations as before (Fig;. 232).


It chondrifies separately from the vertebral body and earlier. Except in the case of the first vertebra it fuses subsequently with the remainder of the vertebral body, and disappears as


THE SKELETOX


417


a separate component. Schauinsland has interpreted it as the homologue of the haemal arches of reptilia {e.g., Sphenodon).

The membrane represents not only the future bony parts but the ligaments and periosteum as well. Hence we find that the successive membranous vertebrae are not separate structures but are united by membrane, i.e., condensed mesenchyme, and are distinguishable from the future ligaments at first only by greater condensation. In the stage of Fig. 233, chondrification has already begun in the vertebral body, hence there is a sharp


/v'a


Fig. 235. — Median sagittal section of the cervical region at

the end of the sixth day of incubation. (After Froriep.) x 40.

b. C, Basis cranii. iV. L. 1, 2, 3, First, second, and third intervertebral ligaments, s. n. b. 1, 2, 3, 4, First, second, third, and fourth subnotochordal bars (hypocentra). v. C. 3, 4, Pleurocentra of third and fourth vertebrae.


distinction in this region l^etween the vertebral bod}^ and intervertebral discs. The centers of chondrification, however, grade into the membranous costal processes and neural arches.

The vertebral segmentation has now become predominant as contrasted with the primitive somitic.

The development of the vertebrae during the fifth day comprises: (1) Fusion of successive caudal and cephalic divisions of


418 THE DEVELOPMENT OF THE CHICK

the sclerotomes to form the definitive vertebrae; (2) union of the cephaUc vertebral components beneath the notochord to form the subnotochordal bar; (3) origin of the membranous vertebral bodies and of the neural arch and costal processes.

Chondrification, or development of cartilage, sets in from the following centers in each vertebra: (1) the cephalic neural arches and subnotochordal bar, forming a horseshoe-shaped cartilage at the cephalic end of each vertebra; (2) and (3) right and left centers in the body of each vertebra behind the subnotochordal bar, which soon fuse around the notochord; (the subnotochordal bar probably corresponds to the hypocentrum, and the lateral centers (2 and 3) to the pleurocentra of palaeontologists) ; (4) and (5) centers in each costal process (Figs. 235 and 236). These centers are at first separated by membrane, l)ut except in the case of the costal processes, which form the ribs, the cartilage centers flow together. The neural arches end in membrane which gradually extends dcrsally around the upper part of the neural tube, finally uniting above with the corresponding arches of the other side to form the memhrana reuniens. The chondrification follows the extension of the membrane. During this time the transverse processes of the neural arch and the zygopophyses are likewise formed as extensions of the membrane.

The distinction that some authors make between a primary vertebral l^ody formed ]:)y chondrification within the perichordal sheath, and a secondary vertebral body formed by the basal ends of the arches surrounding the primary, is not a clear one in the case of the chick.

On the seventh and eighth days the process of chondrification extends into all parts of the vertebra; the entire vertebra is, in fact, laid down in cartilage on the eighth da}', although the neural spine is somewhat membranous. Fig. 237 shows the right side of four trunk vertebrae of an eight-day chick, prepared according to the methylene b,lue method of Van Wijhe. The


Fig. 236. — Frontal section of the vertebral column and neighboring structures of a 6-day chick. Upper thoracic region. Note separate centers of chondrification of the neural arch, centrum, and costal processes. Anterior end of section above. B. n. A., Base of neural arch. br. N. 1, 2, 3, First, second, and third brachial nerves. Cp. R., Capitulum of rib. iv. D., Intervertebral disc. Mu., Muscles. N. A., Neural arch. T. R., Tuberculum of rib. V. C, Centrum of vertebra. Other abbreviations as before.


THE SKELETON


419



--jV.D.


420


THE DEVELOPMENT OF THE CHICK


notochord runs continuously through the centra of the four vertebrae shown. It is constricted intra vertebrally and expanded intervertebrally, so that the vertebral bodies are amphicoelous. The intervertebral discs are not shown. A pre- and postzygapophysis is formed on each arch. It is by no means certain that the parts separated by the clear streak shown in the figure extending through centra and arches correspond to the sclerotomal components of the primitive vertebrae, though this was the interpretation of Schauinsland as shown in the figure; further study seems necessary to determine the exact relations of the primitive sclerotomal components to the parts of the definitive vertebra. The successive vertebrae have persistent membranous



Fig. 237. — The right side of four bisected vertebrse of the trunk

of an 8-day chick. (After Schauinsland.)

caud. V. A., Caudal division of vertebral arch. ceph. v. A., Cephalic division of vertebral arch. N'ch., Xotochord.

connections in the regions of the neural spines, zygapophyses and centra. These are shown in Figs. 238 and 239 (cf. also Fig. 150) ; they are continuous with the perichondrium and all are derived from unchondrified parts of the original membranous vertebrae.

Atlas and Axis (epistropheus). The first and second vertebrae agree with the others in the membranous stage. But, when chondrification sets in, the hypochordal bar of the first vertebra does not fuse with the body, but remains separate and forms its floor (Figs. 238 and 239). The body of the first vertebra chondrifies separately and is attached by membrane to the anterior end of the body of the second vertebra, representing in fact the odontoid process of the latter. It has later a separate center of ossification, but fuses subsequently wdth the body of the second vertebra, forming the odondoid process (Fig. 240).


THE SKELETON


421


Formation of Vertebral Articulations. In the course of development the intervertebral discs differentiate into a peripheral intervertebral ligament and a central suspensory ligament which at first contains remains of the notochord. There is a synovial cavity between the intervertebral and suspensory ligaments. This differentiation takes place by a process of loosening and resorption



Fig. 238. — Median sagittal section of the basis

cranii and first three vertebral centra of an

8-day chick.

B. C, Basi-cranial cartilage, iv. D. 1, 2, 3, 4,

First, second, third, and fourth intervertebral

discs. N. T., Floor of neural tube. s. n. b. 1, 2,

First and second subnotochordal bars. V. C.

1, 2, 3, First, second, and third pleurocentra.

of cells just external to the perichordal sheath (Fig. 241). The intervertebral ligament takes the form of paired, fibrous menisci, or, in other words, the intervertebral ligaments are incomplete around the bodies of the vertebrae dorsally and ventrally (Schwarck). Ossification is well advanced in the clavicles, long bones,


422


THE DEVELOPMENT OF THE CHICK


and membrane bones of the skull before it begins in the vertebrae. It takes place in antero-posterior order, so that a series of stages may be followed in a single embryo (cf. Fig. 242). There are three main centers for each vertebra, viz., one in the body and one in each neural arch. The ossification of the centrum is almost




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PiQ 239. — Lateral sagittal section of the same vertebrse (as in Fig.

238). At 1, 2, Floor and roof of atlas. B. C, Basis cranii. Cerv. n. 1, 2, First and second cervical nerves. Med. Obi., Medulla oblongata. R. V. 2, 3, 4, Ribs of the second, third, and fourth vertebrse. V . A. 2, 3, Arches of the second and third vertebrse. XII 2, Second root of hypoglossus.

entirely endochondral, though traces of perichondral ossification may be found on the ventral and dorsal surfaces of each centrum before the endochondral ossification sets in. The perichondral centers soon cease activity. The endochondral centers arise just outside the perichordal sheath near the center of each vertebra on each side of the middle line, but soon fuse around the


THE SKELETON


423


notochord, and rapidly spread in all directions, but particularly towards the surface, leaving cartilaginous ends (Fig. 241). The notochord is gradually reduced and exhibits two constrictions



Fig. 240. — The first cervical vertebrae of a young

embryo of Haliplana fuliginosa. (After Schauins land.)

s.n.b. 1,2, First and second subnotochordal bars. R. 3, 4, 5, 6, Ribs of the third, fourth, fifth, and sixth cervical vertebrae.


and three enlargements within each centrum. The main enlargement occupies the center and the two smaller swellings the cartilaginous ends, the constriction occurring at the junction of the ossified areas and cartilaginous ends (Fig. 241).










J


Fig. 241. — Section through the body of a cervical vertebra of a chick embryo of about 12 days. (After Schwarck.)

1, Endochondral ossification. 2, Articular cartilages. 3, Notochord. 4, Loosening of cells of the intervertebral disc, forming a synovial cavity. 5, Periosteum. 6, Ligamentum suspensorium surrounding the notochord.


424 THE DEVELOPMENT OF THE CHICK

The centers of ossification in the neural arches arise from tlie perichondrium a short distance above the body of the vertebra, and form bony rings about the cartilaginous arch. They gradually extend into all the processes of the neural arch. Thus the neural arches are separated from the vertebral centra by a disc of cartilage which is, however, finally ossified, fusing the arches and centra. At what time this occurs, and at what time endochondral ossification begins in the arches, is not known exactly for the chick.

The vertebral column of birds is characterized by an extensive secondary process of coalescence of vertebrae. Thus the two original sacral vertebra? coalesce with a considerable number of vertebrae, both in front and behind, to form an extensive basis of support for the long iliac bones. The definitive sacrum may be divided into an intermediate primary portion composed of two vertebrge, an anterior lumbar portion, and a posterior caudal portion. The development of these fusions has not been, apparently, worked out in detail for the chick. The bony centers are all separate on the sixteenth day of incubation (cf. Fig. 249). Similarly, the terminal caudal vertebrae fuse to form the so-called pygostyle, which furnishes a basis of support for the tail feathers.

III. Development of the Ribs and Sternal Apparatus In the membranous stage of the vertebral column, all of the trunk vertebra? possess membranous costal processes the subsequent history of which is different in different regions. In the cervical region these remain relatively short, and subsequently acquire independent centers of chondrification and ossification. The last two cervical ribs, however, acquire considerable length. In the region of the thorax, the membranous costal processes grow ventralward between the successive myotomes and finally unite in the formation of the sternum (q.v.). In the lumbar and sacral regions the membranous costal processes remain short. The primary costal process is an outgrowth of the membranous centrum, corresponding in position to the capitulum of the definitive ril). The tuberculum arises from the primary costal process while the latter is still in the membranous condition and grows dorsal ward to unite with the neural arch in the region of the transverse process. (See Fig. 236.)

The centers of chondrification and ossification of the typical


THE SKELETON 425

ribs (cervical and thoracic) arise a short distance lateral to the vertebral centers, with which they are connected only by the intervening membrane, which forms the vertebro-costal ligaments. Chondrification then proceeds distally.

The cervical ribs chondrify from a single center. The thoracic ribs have two centers of chondrification; a proximal one, corresponding to the vertebral division of the rib. and a distal one corresponding to the sternal division. The lumbar and sacral membranous costal processes do not chondrify separately from the vertebral bodies; if they persist at all, therefore, they appear as processes of the vertebrae, and are not considered further.

In the fowl the atlas does not bear ribs, and in the embryo the primary costal processes of this vertebra do not chondrify. The second to the fourteenth vertebrae bear short ribs, with capitulum and tuberculum bounding the vertebrarterial canal. The fourteenth is the shortest of the cervical series. The fifteenth and sixteenth vertebrae bear relatively long ribs, but, as these do not reach the sternum, they are classed as cervical. The entire embryonic history, however, puts them in the same class as the following sternal ribs; on an embryological basis they should be classed as incomplete thoracic ribs. They possess no sternal division, but the posterior one has an uncinate process like the true thoracal ribs. The following five pairs of ribs (vertebrae 17-21) possess vertebral and sternal portions, but the last one fails to reach the sternal rib in front of it.

The vertebral and sternal portions of the true thoracal ribs meet at about a right angle in a membranous joint. This bend is indicated in the membranous stage of the ribs.

The membranous ribs growing downwards and backwards in the wall of the thorax make a sudden bend forward, and their distal extremities fuse (seven and eight days) in a common membranous expansion (primordium of the sternum), which, however, is separated from the corresponding expansion of the opposite side bv a considerable area of the body-wall.

The vertebral and sternal portions of the ribs ossify separately; the ossification of the ribs is exclusively perichondral up to at least the sixteenth day (cf. Fig. 242).

The uncinate processes were not formed in any of the embryos studied. Apparently they arise as separate membranous ossifications after hatching.

The sternum takes its origin from a pair of membranous expan


426


THE DEVELOPMENT OF THE CHICK


sions formed by the fusion of the distal ends of the first four true thoracal ribs; the fifth pair of thoracal ribs does not take part in the formation of the sternum. The sternum thus arises as two distinct halves, which lie at first in the wall of the thorax at the posterior end of the pericardial cavity (eight days). The greatest extension of the sternal primordia is do rso- ventral, the



Fig. 242. — Photograph of the skeleton of a 13-day chick embryo. Prepared by the potash method. (Preparation and photograph by Roy L. Moodie.) 1, Premaxilla. 2, NasaL 3, lachrymaL 4, Parasphenoid. 5, Frontal. 6, Squamosal. 7, Parietal. 8, Exoccipital. 9, Cervical rib. 10, Coracoid. 11, Scapula. 12, Humerus. 13, Ilium. 14, Ischium. 15, Pubis. 16, Metatarsus. 17, Tibiofibula. 18, Palatine. 19, Jugal. 20, Maxilla. 21, Clavicle.

ventral extremities corresponding to the anterior end of the definitive sternum, which is formed by concrescence of the lateral halves in the middle line beginning at the anterior end. The concrescence


THE SKELETON 427

then proceeds posteriorly, as the dorsal ends of the priraordia rotate backwards and downwards towards the middle line.

Although there are two lateral centers of chondrification, these soon fuse. The carina arises as a median projection very soon after concrescence in any region, and progresses backwards, rapidly following the concrescence. There is, therefore, no stage in which the entire sternum of the chick is ratite, though this condition exists immediately after concrescence in any region. The various outgrowths of the sternum (episternal process, anterolateral and abdominal processes), arise as processes of the membranous sternum and do not appear to have independent centers of chondrification.

The sternum ossifies from five centers, viz., a median anterior center and paired centers in the antero-lateral and abdominal processes. The last appear about the seventeenth day of incubation. On the nineteenth day a point of ossification appears at the base of the anterior end of the keel. At hatching centers also appear in the antero-lateral processes. The centers gradually extend, but do not completely fuse together until about the third month. The posterior end of the median division of the sternum remains cartilaginous for a much longer period. In the duck and many other birds there are only two lateral centers of ossification; the existence of five centers in the chick is, therefore, probably not a primitive condition.

IV. Development of the Skull

The skull arises in adaptation to the component organs of the head, viz., the brain, the sense organs (nose, eye, and ear) and cephalic visceral organs (oral cavity and pharynx); it thus consists primarily of a case for the brain, capsules for the sense organs, and skeletal bars developed in connection with the margins of the mouth and the visceral arches. In the chick, the primordia of the auditory and olfactory capsules are continuous ab initio with the primordial cranium; the protecting coat of the eye (sclera) never forms part of the skull. Therefore, we may consider the development of the skull in two sections, first the dorsal division associated with brain and sense organs (neurocranium), and second, the visceral division or splanchnocranium. Although the investment of the eyes forms no part of the skull, yet the eyes exert an immense effect on the form of the skull.


428 THE DEVELOPMENT OF THE CHICK

Development of the Cartilaginous or Primordial Cranium.

(1) The Neurocranium. The neurocranium is derived from the mesenchyme of the head, the origin of which has been described previously. The mesenchyme gradually increases in amount and forms a complete investment for the internal organs of the head. It is not all destined, however, to take part in the formation of the skeleton, for the most external portion forms the derma and subdermal tissue; and, internal to the skeletogenous layer, the membranes of the brain and of the auditory labyrinth, etc., are formed from the same mesenchyme.

The notochord extends forward in the head to the hypophysis (Figs. 67, 88, etc.), and furnishes a basis for division of the neurocranium into chordal and prechordal regions. Within the chordal division again, we may distinguish pre-otic, otic, and post-otic regions according as they are placed in front of, around, or behind the auditory sac. The part of the postotic region behind the vagus nerve is the only part of the neurocranium that is primarily segmental in origin. The sclerotomes of the first four somites (Figs. 63 and 117) form this part of the skull; and at least three neural arches, homodynamous with the vertebral arches, are formed in an early stage, but fuse together while still membranous, leaving only the two pairs of foramina of the twelfth cranial nerve as evidence of the former segmentation. It is also stated that membranous costal processes are found in connection with these arches, but they soon disappear without

chondrifying.

The primordial neurocranium is performed in cartilage and corresponds morphologically to the cranium of cartilaginous fishes. However, it never forms a complete investment of the brain; except in the region of the tectum synoticum it is wide open dorsally and laterally. It is subsequently replaced by bone to a very great extent, and is completed and reinforced by numerous membrane bones.

The neurocranium takes its origin from two quite distinct primordia situated below the brain, viz., the parachordals and the trabecular. The former develop on each side of and around the notochord, being situated, therefore, behind the cranial flexure and beneath the mid- and hind-brain; the trabeculae are prechordal in position, being situated beneath the twixt-brain and cerebral hemispheres, and extending forward through the


THE SKELETON 429

interorbital region to the olfactory sacs. It is obvious, therefore, that the parachordals and trabeculse must form with relation to one another the angle defined by the cranial flexure.

The parachordals appear in fishes as paired structures on either side of the notochord, uniting secondarily around the latter; but in the chick the perichordal portion is formed at the same time as the thicker lateral portions, so that the parachordals exist in the form of an unpaired basilar plate from the first. The trabeculae are at first paired (in the earliest membranous condition), but soon fuse in front, while the posterior ends form a pair of curved limbs (fenestra hypophyseos) that surrounds the infundibulum and hypophysis, and joins the basilar plate behind the latter. At the same time that the parachordals and trabeculae are formed by condensations of mesenchyme, the latter condenses also around the auditory sacs and olfactory pits in direct continuity with the parachordals and trabeculae respectively; so that the auditory and olfactory capsules are in direct continuity with the base of the neurocranium from the beginning.

Chondrification begins in the primordial cranium about the sixth day; it appears first near the middle line on each side, and extends out laterally. Somewhat distinct centers corresponding to the occipital sclerotomes may be found in some birds, but they soon run together, and the entire neurocranium forms a continuous mass of cartilage (sixth, seventh, and eighth days).

During this process the trabecular region increases greatly in length simultaneouslv with the outgrowth of the facial region, and the angle defined by the cranial flexure becomes thus apparently reduced. The posterior border of the fenestra hypophyseos marks the boundary between the basilar plate and trabecular region.

In the region of the basilar plate the following changes take place: (1) in the post-otic or occipital region a dorso-lateral extension (Fig. 244) fuses with the hinder portion of the otic capsule, thus defining an opening that leads from the region of the cavity of the middle ear into the cranial cavity (fissure metotica). This expansion is pierced by the foramina of the ninth tenth and eleventh nerves. (2) The otic region becomes greatly expanded by the enlargement of the membranous labyrinth. The cochlear process grows ventrally and towards the middle line and thus invades the original parachordal region (Fig. 168). The


430 THE DEVELOPMENT OF THE CHICK

posterior region of the otic capsule expands dorsally above the hind-brain, and forms a bridge of cartilage extending from one capsule to the other, known as the tectum synoticum (Fig. 244, 33). (3) The preotic region expands laterally and dorsally in the form of a wide plate (alisphenoidal plate) which is expanded transversely, and thus possesses an anterior face bounding the orbit posteriorly and a posterior face forming part of the anterior wall of the cranial cavity. This plate arises first between the ophthalmic and maxillo-mandibular branches of the trigeminus, and subsequently sends a process over the latter that fuses with the anterior face of the otic capsule, thus establishing the foramen prooticum.

For an account of numerous lesser changes, the student is referred to Gaupp (1905), and the special literature (especially Parker, 1869). The various foramina for the fifth to the twelfth cranial nerves are defined during the process of chondrification ; the majority of these are shown in the figures.

The trabecular region may be divided into interorbital and ethmoidal (nasal) regions. The basis of the skeleton in this region is formed by the trabecule alread}^ described. The median plate formed by fusion of the trabeculse extends from the pituitary space (fenestra hypophyseos) to the tip of the head; a high median keel-like plate develops in the interorbital and internasal regions

Fig. 243. — Skull of an embryo of 65 mm. length; right side. Membrane bones in yellow. Cartilage in blue. (Drawn from the model of W. Tonkoff ; made by Ziegler.)

Fig. 244. — View of the base of the same model.

24.3-244. — 1, Squamosum. 2, Parietale. 3, Capsula auditiva. 4, Capsula auditiva (cochlear part). 5, Fissura metotica. 6, Epibranchial cartilage. 7, Sphenolateral plate. 8, Foramen prooticum. 9, Columella. 10. Otic process of quadratum. 11, Basitemporal (postero-lateral part of the parasphenoid). 12, Articular end of Meckel's cartilage. 13, Angulare. 14, Supra-angulare. 15, Dentale. 16, Skeleton of tongue. 17, Pterygoid. 18, Palatine. 19, Rostrum of parasphenoid. 20, Quadrato-jugal. 21, Jugal (zygomaticum). 22, Vomer. 23, Maxilla. 24, Premaxilla. 25, Anterior turbinal. 26, Posterior turbinal. 27, Nasale. 28, Prefrontal (lachrymale). 29, Antorbital plate. 30, Interorbital foramen. 31, Interorbital septum. 32,Frontale. 33, Tectum synoticum. 34, Foramen magnum. 35, Prenasal cartilage. 36, Orbital process of quadrate. 37, Articular process of Quadrate. 38. Fenestra basicranialis posterior. 39, Chorda. IX, Foramen glossopharyngei. X, Foramen vagi. XII, Foramina hypoglossei.

Fig. 245. — Visceral skeleton of the same model.

1, Dentale. 2, Operculare. 3, Angulare. 4, Supra-angulare. 5. Meckel's cartilage. 6, Entoglossum (cerato-hyal). 7, Copula (1). 8, Pharyngobranchial (1). 9, Epibranchial. 10, Copula (2),


3?


30


3^y



f/g 243



f/"g t45


T,^


a4^


THE SKELETON 431

and fuses with the trabeculse, forming the septum interorbitale and septum nasi (Fig. 243). The free posterior border of this plate hes in front of the optic nerves; an interorbital aperture arises in tlie plate secondarily (Fig. 243).

In the ethmoidal region the septum nasi arises as an anterior continuation of the interorbital plate; and the trabecular plate is continued forward as a prenasal cartilage in front of the olfactory sacs. Curved, or more or less rolled, plates of cartilage develop in the axis of the superior, middle, and inferior turbinals (see olfactory organ), and these are continuous with the lateral wall of the olfactory capsules, which in its turn arises from the dorsal border of the septum nasi (Figs. 243 and 244).

(2) The Origin of the Visceral Chondrocranium (Cartilaginous Splanchnocranium) . The visceral portion of the cartilaginous skull arises primarily in connection with the arches that bound the cephalic portion of the alimentary tract, viz., oral cavity and pharynx. In the chick, cartilaginous bars are formed in the mandibular arch, hyoid arch, and third visceral arch. In fishes, the posterior visceral arches also have an axial skeleton, but hi the chick the mesenchyme of these arches does not develop to the stage of cartilage formation. The elements of these arches are primarily quite distinct. The upper ends of the mandibular and hyoid skeletal arches are attached to the skull; and the lower ends of the three arches concerned meet in the middle line. Two medial elements or copulse are formed in the floor of the throat, one behind the angle of the hyoid arch, and one behind the third visceral arch (Fig. 245).

Mandibular Arch. Two skeletal elements arise in the mandibular arch on each side, a proximal one (the palato-quadrate) and a distal one (Meckel's cartilage). The former is relatively compressed, and the latter an elongated element (Fig. 243, 10). The palato-quadrate lies external to the antero-vertral part of the auchtory capsule, and soon develops a triradiate form. The processes are: the processus oticus, which applies itself to the auditory capsule, the processus articidaris, which furnishes the articulation for the lower jaw, and the processus orhitalis, Avhich is directed anteromedially towards the orbit. A small nodule of cartilage of unknown significance lies above the junction of the processus oticus and otic labyrinth. Meckel's cartilage is the primary skeleton of the lower jaw, corresponding


432 THE DEVELOPMENT OF THE CHICK

to the definitive lower jaw of selachians. It consists of two rods of cartilage in the rami of the mandibular arch, which articulate proximally with the processus articularis of the palatoquadrate cartilage,, and meet distally at the symphysis of the lower jaw. The form of the articulation of the lower jaw is early defined in the cartilage (seven to eight days).

Hyoid Arch. The skeletal elements of the hyoid arch consist of proximal and distal pieces (with reference to the neurocranium) which have no connection at any time. The former are destined to form the columella, and the latter parts of the hyoid apparatus. The columella apparently includes two elements (in Tinnunculus according to Suschkin, quoted from Gaupp) : a dorsal element, interpreted as hyomandibular, in contact with the wall of the otic capsule, and a small element (stylohyal) beneath the former. The two elements fuse to form the columella, the upper end of which is shown in Fig. 168. The stapedial plate (operculum of the columella) is stated to arise in Tinnunculus from the wall of the otic capsule, being cut out by circular cartilage resorption and fused to the columella.

The distal elements of the hyoid arch consist of (1) a pair of ceratohyals, which subsequently fuse in the middle line to form the entoglossal cartilage, the proximal ends remaining free as the lesser cornua of the hyoid, and (2) a median unpaired piece (copula I or basihyal) behind the united ceratohyals (Fig. 245).

First Branchial Arch. The skeletal elements of the third visceral (first branchial) arch are much more extensive than those of the hyoid arch. They are laid down as paired cerato- and epi-branchial cartilages on each side, and an unpaired copula II (basibranchial I) in the floor of the pharynx, in the angle of the other elements (Fig. 245). The cerato- and epibranchials increase greatly in length, and form the long curved elements (greater cornua) of the hyoid, which attain an extraordinary development in many birds.

Ossification of the Skull. The bones of the skull are of two kinds as to origin: (1) those that arise in the primordial cranium, and thus replace cartilage (cartilage bones or replacement bones), and (2) those that arise by direct ossification of membrane (membrane or covering bones).

The cartilage bones of the bird's skull are: (a) in the occipital region; the basioccipital, two exoccipitals, and the supraoccipitals; {h) in the otic region: prootic, epiotic, and opisthotic;


THE SKELETON 433

(c) in the orbital region: the basisphenoid, the orbitosphenoids, the ahsphenoids and ossifications of the interorbital septum; (d) in the ethmoidal region the bony ethmoidal skeleton; (e) the palatoquadrate cartilage furnishes the quadrate bone; (/) a proximal ossification, the articulare, arises in Meckel's cartilage and fuses later with membrane bones; (g) the upper part of the hyoid arch furnishes the columella, and the ceratohyals the os entoglossum; (h) the cerato- and epibranchials ossify independently, as also do the two copulse. (See Figs. 243, 244 and 245.)

The membrane bones of the skull are: (a) in the region of the cranium proper: parietals, frontals, squamosals; (6) in the facial region: lachrymals, nasals, premaxillae, maxillae, jugals, quadrato-jugals, pterygoids, palatines, parasphenoid, and vomer; (c) surrounding Meckel's' cartilage and forming the lower jaw: angulare, supra-angulare, operculare, and dentale. (See Figs. 243, 244 and 245.)

The embryonic bird's skull is characterized by a wealth of distinct bones that is absolutely reptilian; but in the course of development these fuse together so completely that it is only in the facial and visceral regions that the sutures can be distinguished readily.

In order of development the membrane bones precede the cartilage bones, though the latter are phylogenetically the older. Thus, about the end of the ninth day, the following bones are present in the form of delicate reticulated bars and plates: all four bones of the mandible, the faint outline of the premaxillae, the central part of the maxillae, the jugal and quadratojugal, the nasals, the palatines and pterygoids. The base of the squamosal is also indicated by a small triangular plate ending superiorly in branching trabeculae, delicate as frost-work. A faint band of perichondral bone is beginning to appear around the otic process of the quadrate, the first of the cartilage bones to show any trace of ossification. These ossifications appear practically simultaneously as shown by the examination of the earlier stages.

On the twelfth day these areas have expanded considerably, and the frontals and prefrontals (lachrymals) are formed; the rostrum of the parasphenoid is also laid down, and the exoccipitals appear in the cartilage at the sides of the foramen magnum. The parietals appear behind the squamosal (Fig. 242) about the thirteenth day; the basioccipitals soon after. The supraoc


434 THE DEVELOPMENT OF THE CHICK

cipital appears as a pair of ossifications in the tectum synoticum on each side of the dorsal middle line, subsequently fusing together.

A detailed history of the mode of ossification of all the various bones of the skull would be out of place in this book. The figures illustrate some points not described in the text. The reader is referred to W. K. Parker (1869) and to Gaupp (1905).

V. Appendicular Skeleton

The appendicular skeleton includes the skeleton of the limbs and of the girdles that unite the limbs to the axial skeleton. The fore and hind-limbs, being essentially homonymous structures, exhibit many resemblances in their development.

The Fore-limb. The pectoral girdle and skeleton of the wing develop from the mesenchyme that occupies the axis and base of the w^ng-bud, as it exists on the fourth day of incubation. It is probably of sclerotomic origin, but it is not known exactly how many somites are concerned in the chick, nor which ones. After the wing has gained considerable length (fifth day) it can be seen from the innervation that three somites are principally involved in the wing proper, viz., the fourteenth, fifteenth, and sixteenth of the trunk. But it is probable that the mesenchyme of the base of the wing-bud, from which the pectoral girdle is formed, is derived from a larger number of somites.

It is important, then, to note first of all that the scapula, coracoid, clavicle, humerus, and distal skeletal elements of the wing are represented on the fourth day by a single condensation of mesenchyme, which corresponds essentially to the glenoid region of the definitive skeleton. From this common mass a projection grows out distally in the axis of the wing-bud, and three projections proximally in different directions in the bodywall. These projections are (1) the primordium of the wingskeleton, (2) of the scapula, (3) of the coracoid, (4) of the clavicle.

The Pectoral Girdle. The elements of the pectoral girdle are thus outgrowths of a common mass of mesenchyme. The scapula process grows backward dorsal to the ribs; the coracoid process grows ventralward and slightly posterior towards the primordium of the sternum, thus forming an angle slightly less than a right angle with the scapular process; and the clavicular process grows


THE SKELETON 435

out in front of the coracoid process ventrally and towards the middle hne. ThevSe processes are quite well developed on the fifth day, and increase considerably in length on the sixth day, when the hind end of the scapula nearly reaches the anterior end of the ilium, and the lower end of the coracoid is very close to the sternum. The elements are still continuous in the glenoid region.

About the end of the sixth day independent centers of chondrification appear in the scapula and coracoid respectively near their imion; these spread distally and fuse centrally, so that on the seventh day the coraco-scapula is a single bent cartilaginous element. In the angle of the bend, however (the future coraco-scapular joint), the cartilage is in a less advanced condition than in the bodies of the two elements. The clavicular process, on the other hand, never shows any trace of cartilage formation, either in early or more advanced stages, but ossifies directly from the membrane. It separates from the other elements of the pectoral girdle, though not completel}', on the eighth dav.

The scapula and coracoid ossify in a perichondral fashion, beginning on the twelfth da}^, from independent centers, which approach but never fuse, leaving a permanent cartilaginous connection (Fig. 242). The clavicle, on the other hand, is a purely membrane bone; bony deposit begins in the axis of the membranous rods on the eighth or ninth days, soon forming fretted rods that approach in the mid-ventral line by enlarged ends, which fuse directly without the intervention of any median element about the twelfth to thirteenth day, thus forming the furcula or wish-bone (Fig. 246).

The nature of the clavicle in birds has been the subject of a sharp difference of opinion. On the one hand, it has been maintained that it is double in its origin, consisting of a cartilaginous axis (procoracoid) on which a true membrane bone is secondarily grafted (Gegenbaur, Fiirbringer, Parker, and others) ; on the other hand, all cartilaginous preformation in its origin has been denied by Rathke, Goette, and Kulczycki. After careful examination of series of sections in all critical stages, and of preparations made by the potash method, I feel certain that in the chick at least there is no cartilaginous preformation. It is still possible (indeed probable on the basis of comparative anatomy) that the theory of its double origin is correct phylogenetically; but it is certain that the


436


THE DEVELOPMENT OF THE CHICK


procoracoid component does not develop beyond the membranous stage in the chick. It is interesting that the clavicle is the first center of ossification in the body, though perichondral ossification of some of the long bones begins almost as soon.

The Wing-bones. The primordium of the wing-bones is found in the axial mesenchyme of the wing-bud, which is originally continuous with the primordium of the pectoral girdle, and shows no trace of the future elements of the skeleton. The differentiation of the elements accompanies in general the external differentiation of the wing illustrated in Figs. 121 to 124, Chapter VII. The humerus, radius, and ulna arise by membranous differentiation in the mesenchyme in substantially their definitive relations; they pass through a complete cartilaginous stage and



Fig. 246. — Photograph of the pectoral girdle of a chick embryo of 274 hours; prepared by the potash method. (Preparation and photograph by Roy L. Moodie.)

1, Coracoid. 2, Clavicle. 3, Scapula. 4, Humerus.


then ossify in a perichondral fashion (see Fig. 242). In the carpus, metacarpus, and phalanges, more elements are formed in the membrane and cartilage than persist in the adult. Elimination as well as fusion takes place. These parts will therefore require separate description.

As birds have descended from pentadactyl ancestors with subsequent reduction of carpus, metacarpus, and phalanges, it is naturally of considerable interest to learn how much of the ancestral history is preserved in the embryology. The hand is represented in the embryo of six days by the spatulate extremity of the fore-limb, which includes the elements of carpus, metacarpus, and phalanges. From this expansion five digital rays grow out simultaneously, the first and fifth being relatively


THE SKELETOX


437


small; the second, third, and fourth represent the persistent digits. In each ray is a membranous skeletal element, which, however, soon disappears in the first and fifth. Thus there are distinct indications of a i^entadactyl stage in the development of the bird's wing.

In the definitive skeleton there are but two carpal bones, viz., a radiale at the extremity of the radius, and an ulnare at the extremity of the ulna. In the embryo there is evidence of seven transitory pieces in the carpus arranged in two rows, proximal and distal (Fig. 247). In the proximal row only two car


M.c.J

M c. 2


^A*"?^


jPcA



-U


M'c.-?^


Cp.^ Cp3 ^•^■


P'c/).


Fig. 247. — Skeleton of the wing of a chick embryo of 8 days. (After W.

K. Parker.)

Cp. 2, 3, and 4, Second, third, and fourth carpalia. C. U., Centraloiilnare. H., Humerus. I. R., Intermedio-radiale. M'c. 2, 3, 4, Second, third, and fourth metacarpalia. P'ch., Perichondral bone R., Radius. U., Ulna.

tilages appear, viz., the radiale and ulnare; but in earlier stages each appears to be derived from two centers: the radiale from a radiale s.s. and an intermedium, the ulnare from an ulnare s.s. and a centrale. Evidence of such double origin of each is found also in the cartilaginous condition {v. Parker, 1888). Four elements in all enter into the composition of this proximal row. In the distal row there are three distinct elements corresponding to the three persistent digits, and representing, therefore, carpalia II, III, and IV. These subsequently fuse with one another, and with the heads of the metacarpals to produce the carpometacarpus.

On the seventh day the metacarpus is represented Ijy three cartilages corresponding to the three persistent digits, viz., II,


438 THE DEVELOPMENT OF THE CHICK

III, IV. Metacarpal II is only about one third the length of III. Metacarpal IV is much more slender than III, and is bowed out in the middle, meeting III at both ends. The elements are at first distinct, but II and III fuse at their proximal ends in the process of ossification. Cartilaginous rudiments of metacarpals I and V have also been found by Parker, Rosenberg, and Leighton. As to the phalanges, Parker finds two cartilages in II, three in III, and two in IV on the seventh day; but already on the eighth day the distal phalanges of III and I^' have fused with the next proximal one.

As regards the homology of the digits of the wing, the author has adopted the views of Owen, Mehnert, Norsa, and Leighton, that they represent numbers II, III, and IV, which seem to be better supported by the embryological evidence than the view of ^Meckel, Gegenbauer, Parker, and others, that they represent I, II, and HI.

The Skeleton of the Hind-limb. The skeleton of the hindlimb and pelvic girdle develops from a continuous mass of mesenchyme situated at the base of the leg-bud. The original center of the mass represents the acetabular region; it grows out in four processes: (1) a lateral projection in the axis of the leg-bud, the primordium of the leg-skeleton proper, (2) a dorsal process, the primordium of the ilium; and two diverging ventral processes, one in front of the acetabulum (3) the pubis, and one behind (4) the ischium. In the membranous condition the elements are continuous. The definitive elements develop either as separate cartilao-e centers in the common mass (usually), or as separate centers of ossification in a common cartilaginous mass (ilium

and ischium).

The Pelvic Girdle. The primitive relations of the elements of the pelvic girdle in Larus ridibundus is shown in Fig. 248, which represents a section in the sagittal plane of the body, and thus does not necessarily show the full extent of any of the cartilaginous elements, but only their general relations. The head of the femur is seen in the acetabulum, the broad plate of the ilium above and the pubis and ischium as cartilaginous rods of almost equal width below, the pubis in front and the ischiimi behind the acetabuhmi. In this stage the pehdc girdle, in this and many other species of birds, consists of three separate elements on each side in essentially reptilian relations.


THE SKELETOX


439


In the chick at a corresponding age the ihum is much more extensive, and the ischium is united with it by cartilage- the pubis, however, has only a membranous connection with the ilium (contra Johnson). In the course of development the distal ends of the ischium and pubis rotate backwards until the two elements come to lie substantially parallel to the ilium (Figs. 242 and 249). The displacement of the ischium and pubis may


//.


u^


'^lx'~^^'~^i


/s.n.


Is.


Cr.N.


oi.JV.


Fig. 248. — Sagittal section of the right half of the body of Lams ridibundus, to show the composition of the pelvic girdle; x 35. Length of the leg-bud of the embryo, 0.4 mm. (After Mehnert.) F., Femur, cr. N., Crural nerve. II., Ihum. I. s., Ischium. Is. N., Ischial nerve, ob. N., Obturator nerve. P., Pubis.

be associated wdth the upright gait of birds; it is fully established on the eighth day in the chick. The mode of ossification, which is perichondral, is shown in Fig. 249.

Later, the ilium obtains a very extensive pre- and postacetabular union with the vertebrae. I have fomid no evidence in a complete series of preparations (potash) of attachment by ribs arising as indei^endent ossifications. The ischium also fuses


440


THE DEVELOPMENT OF THE CHICK


with the ventral posterior border of the iUum, and the pubis,

except at its anterior and posterior ends, with the free border

of the ischium.

The spina iliaca, a pre-acetabular, bony process of the ihum,

requires special mention inasmuch as it has been interpreted (by Marsh) as the true pubis of birds, and the element ordinarily named the pubis as homologous to the post-pubis of some reptiles. There is no evidence for this in the development. The spina iliaca develops as a cartilaginous outgrowth of the ilium and ossifies from the latter, not from an independent center (Mehnert).

The Leg-skeleton. The skeleton of the leg develops from the axial mesenchyme, which is at first continuous with the primordium of the pelvic girdle. In the process of chondrification it segments into a larger number of elements than found in the adult, some of which are suppressed and others fuse together. The digits grow out from the palate-like expansion of the primitive limb in the same fashion as in the wing. In general the

separate elements arise in the proximo-distal order (Figs. 242 and

249)..

The femur requires no special description; ossification begins

on the ninth day.

The primordium of the fibula is from the first more slender than that of the tibia, though relatively far larger than the adult



Fig. 249. — Photograph of the skeleton

of the leg of a chick embryo of 15 days'

incubation. Prepared by the potash

method. (Preparation and photograph

by Roy L. Moodie.)

1, Tibia. 2, Fibula. 3, Patella. 4, Femur. 5, Ilium. 6, Pleurocentra of sacral vertebrae. 7, Ischium. 8, Pubis. 9, Tarsal ossification. 10, Second, third, and fourth metatarsals. 11, First metatarsal. I, II, III, IV, First, second, third, and fourth digits.


THE SKELETON


441


fibula. The fibular cartilage extends the entire length of the crus, but ossification is confined largely to its proximal end; on the fourteenth day its lower half is represented by a thread-like filament of bone. '

No separate tarsal elements are found in the adult; but in the embryo there are at least three cartilages, viz., a fibulare, tibiale and a large distal element opposite the three main metatarsals. In the course of development, the two proximal elements fuse with one another, and with the distal end of the tibia. The distal element fuses with the three main metatarsals, first with the second, then with the fourth, and lastly with the third (Johnson).

Five digits are formed in the membranous stage of the skeleton. In the case of the fifth chgit, only a small nodule of cartilage (fifth metatarsal) develops and soon disappears. The second, third, and fourth are the chief digits; the first is relatively small. ^Metatarsals 2, 3, and 4 are long and ossify separately in a perichondral fashion. They become applied near their middle and fuse with one another and with the distal tarsal element to form the tarso-metatarsus of the adult (Fig. 250). The first metatarsal is short, lying on the preaxial side of the distal end of the others (Fig. 249); it ossifies after the first phalanx. The number of phalanges is 2, 3, 4, and 5 in the first, second, third, and fourth digits respectively (Fig. 249).

The patella is clearly seen in potash preparations of thirteen-day chicks. At the same time there is a distinct, though iiiiiuite, separate center of ossification in the tarsal region (Fig. 249).



Fig. 250. — Photograph of the skeleton of the foot of a chick embryo of 15 days' incubation. (Preparation and photograph by Roy L. Moodie)

1, 2, 3, 4, First, second, third, and fourth digits. M 2, M 3, M 4, Second, third, and fourth metatarsals.


APPENDIX


GENERAL LITERATURE

V. Baer, C. E., L'eber Entwickelurigsgeschichte der Tiere. Beobachtung

und Reflexion. Konigsbcrg, 1828 u. 1837.

id., 2. Teil — Herausgegeben von Stieda. Konigsberg, 1888. Duval, Mathias, Atlas d'embryologie. (With 40 plates.) Paris, 1889. Foster, M., and Balfour, F. M., The Elements of Embryology. Second

Edition revised. London, 1883. Gadow, Hans, Die Vogel, Bronn's Klassen und Ordniingen des Thier-Reichs,

Bd. VI, Abth. 4, 1898. Handbuch der vergleichenden und experimentellen Entwickelimgslehre der

Wirbeltiere. Edited by Dr. Oskar Hertwig and written by numerous

collaborators. Jena, 1901-1907. Hls, W., LTntersuchungen fiber die erste Anlage des Wirbeltierleibes. Die

erste Entwickelung des Hiihnchens im Ei. Leipzig, 1868. Keibel, F., and Abraham, K., Normaltafeln zur Entwickelungsgeschichte

des Huhnes (Gallus domesticus). Jena, 1900. V. KoLLiKER, A., Entwickelungsgeschichte des Menschen und der hoheren

Thiere. Zweite Aufl. Leipzig, 1879. Marshall, A. M., Vertebrate Embryology. A Text-book for Students and

Practitioners. (Ch. IV, The Development of the Chick.) New York

and London, 1893. MiNOT, C. S., Laboratory Text-book of Embryology. Philadelphia, 1903. Pander, Beitrage zur Entwickelungsgeschichte des Hiihnchens im Ei. Wiirz burg, 1817. Prevost et Dumas, Memoire sur le developpement du poulet dans I'oeuf.

Ann. Sc. Nat., Vol. XII, 1827. Preyer, W., Specielle Physiologic des Embryo. Leipzig, 1885. Remak, R., Untersuchungen iiber die Entwickelung der Wirbelthiere. Berlin, 1855.

LITERATURE — CHAPTER I

Bartelmez, George W., 1912, The Bilaterality of the Pigeon's Egg. A Study in Egg Organization from the First Growth Period of the Oocyte to the Beginning of Cleavage. Journ. of Morph. Vol. 23., pp. 269-328.

CoSTE, M., Histoire generale et particuliere du developpement des corps organises, T. I. (Formation of Egg in Oviduct, see Chap. VI). Paris, 1847-1849.

D 'Hollander, F., Recherches sur I'oogenese et sur la structure et la signification du noyau vitellin de Balbiani chez les oiseaux. Archiv. d'anat. micr., T. VII, 1905.

Gegenbaur, C, Ueber den Bau und die Entwickelung der Wirbeltiereier mit partieller Dottertheilung. Archiv. Anat. u. Phys., 1861.

443


444 APPENDIX

Glaser, Otto, 1913, On the Origin of Double-yolked Eggs. Biol. Bull.,

Vol. 24, pp. 175-186. HoLL, M., Ueber die Reifung der Eizelle des Huhnes. Sitzungsber. Akad Wiss. Wien, math.-nat. KL, Bd. XCIX, Abth. Ill, 1890.

V. Nathusius, W., Zur Bildung der Eihiillen. Zool. Anz. Bd. XIX, 1896.

Die Entwickelung von Schale und Schalenhaut des Hiihnereies im

Ovidukt. Zeitschr. wiss. Zool., Bd. LV, 1893.

Parker, G. H., Double Hen's Eggs. American Naturalist, Vol. XL. 1906.

Pearl, Raymond and Curtis, M. R, 1912, Studies on the Physiology of

Reproduction in the Domestic Fowl. V. Data Regarding the Physiology

of the Oviduct. Journ. of Exp. Zoology. Vol. 12, pp. 99-132. Riddle, Oscar, 1911, On the Formation, Significance and Chemistry of

the White and Yellow Yolk of Ova. Journ. of Morph., Vol. 22, pp.

455-490. SoNNENBRODT, 1908, Die Wachstunsperiode der Oocyte des Huhns. Arch.

f. mikr. Anat. w. Entw. Bd. 72, pp. 415-480. Waldeyer, W., Die Geschlechtszellen. Handbuch der vergl. und exper.

Entwickelungslehre der \Yirbeltiere. Bd. I, T. 1, 1901.

LITERATURE — CHAPTER II

Andrews, E. A., Some Intercellular Connections in an Egg of a Fowl. The Johns Hopkins University Circular. Notes from the Biological Laboratory, March, 1907.

Barfurth, D., Versuche iiber die parthenogenetische Furchung des Hiihnereies. Arch. Entw.-mech., Bd. 2, 1895.

Blount, Mary, The Early Development of the Pigeon's Egg with Especial Reference to the Supernumerary Sperm-nuclei, the Periblast and the Germ-wall. Biol. Bull., Vol. XIII, 1907.

Duval, M., De la formation du l^lastoderm dans Foeuf d'oiseau. Ann. Sc. Nat. Zool., Ser. 6, T. XVIII, 1884.

Gasser, E., Der Parablast und der Keimwall der Vogelkeimscheibe. Sitzungsber. der Ges. zur Beford. d. ges. Naturwiss. zu Marburg, 1883. Eierstocksei und Eileiterei des Vogels. Ibid, 1884.

Gotte, a., Beitrage zur Entwickelungsgeschichte der Wirbeltiere, II. Die Bildung der Keimblatter und des Blutes im Hiihnerei. Archiv. mikr. Anat., Bd. X, 1874.

Harper, E. H., The Fertilization and Early Development of the Pigeon's Egg. Am. Jour. Anat., Vol. Ill, 1904.

KiONKA, H., Die Furchung des Hiihnereies. Anat. Hefte, Bd. Ill, 1894.

Lau, H., Die parthenogenetische Furchung des Hiihnereies. Inaug. Dissert. Jurjew — Dorpat., 1894.

Oellacher, J., Untersuchungen iiber die Furchung und Blatterl)ildung im Hiihnerei. Studien iiber experimentelle Pathologic von Strieker, Bd

I, 1869. Oellacher, J., Die Veranderungen des unbefruchteten Keimes des Huhnereies im Eileiter und bei Bebriitungsversuchen. Zeitschr. wiss. Zool., Bd. XXII, 1872.


APPENDIX 445

Patterson, J. Thomas, Gastrulation in the Pigeon's Egg; a ^Morphological

and Experimental Study. The Journ. of Morph., Vol. 29, pp. 65-123,

1909. Patterson, J. Thomas, Studies on the Early Dev^elopment of the Hen's

Egg. 1. History of the Early Cleavage and of the Accessory Cleavage.

The Journ. of Morph., Vol. 21, pp. 101-134, 1910. Rauber, a., Ueber die Stellung des Hiihnchens im Entwicklungsplan.

Leipzig, 1876. Sobotta, J., Die Reifung und Befruchtung des Wirbeltiereies. Ergeb.

Anat. u. Entwickelungsgesch., Bd. V, 1895.

LITERATURE — CHAPTER III

Edwards, C. L., The Physiological Zero and the Index of Development for

the Egg of the Domestic Fowl, Gallus Domesticus. Am. Journ. Physiol.,

Vol. VI, 1902. Eycleshymer, a. C, Some Observations and Experiments on the Natural

and Artificial Incubation of the Egg of the Common Fowl. Biol. Bull.,

Vol. XII, 1907. Fere, Cm., Note sur I'influence de la temperature sur I'incubation de I'oeuf

de poule. Journ. de I'anatomie et de la physiologic, Paris, T. XXX,

1894.

LITERATURE — CHAPTERS IV AND V

Assheton, R., An Experimental Examination into the Growth of the Blastoderm of the Chick. Proc. Roy. Soc, London, Vol. LX, 1896.

Balfour, F. M. The Development and Growth of the Layers of the Blastoderm. Quar. Jour. Micr. Sc, Vol. XIII, 1873.

On the Disappearance of the Primitive Groove in the Embryo Chick. lUd.

Balfour, F. M., and Deighton, A Renewed Study of the Germinal Layers of the Chick. Quar. Jour. Micr. Sc, Vol. XXII, 1882.

DissE, J., Die Entwickelung des mittleren Keimblattes im Hiihnerei. Arch, mikr. Anat., Bd. XV, 1878.

DuRSY, Emil, Der Primitivstreif des Hiihnchens. Lahr, 1866.

Duval, Mathias, Etudes sur la hgne primitive de rembr3'on du poulet. Ann. Sc. Nat. Zool., Ser. 6, T. VII, 1S7S.

De la formation du blastoderm dans I'oiuf d'oiseau. Ann. Sc. Nat. Zool., Ser. 6, T. XVIII. Paris, 1884.

Evans, Herbert M. On the Development of the Aorta), Cardinal and UmbiUcal Veins and other Blood-vessels of Vertebrate Embryos from Capillaries. Anatomical Record., Vol. 3, pp. 498-518, 1909.

Fol, H., Recherches sur le developpement des protovertcbres chez I'embryon du poulet. Arch. sc. phys. et nat. Geneve, T. II, 1884.

Gasser, Lieber den Primitivstreifen bei Vogelembryonen. Sitz.-Ber. d. Gcs. z. Beforcl. d. ges. Naturw. z. Marburg, 1877.

Der Primitivestreif bei Vogelembryonen (Huhn w. Gans). Schriften d. Ges. z. Beford. d. ges. Naturw. z. Marburg, Bd. XI, Suppl. Heft 1, 1879.


446 APPENDIX

Gasser, Beitrage zur Kenntnis der Vogelkeimscheibe. Arch. Anat. u

Entw., 1882.

Der Parablast unci der Keimwall der Vogelkeimscheibe. Sitz.-Ber.

d. Ges. z. Beford. d. ges. Naturw. z. Marburg, 1883. GoETTE, A., Beitrage zur Entwickelungsgeschichte der Wirbeltiere. II.

Die Bildung der Keimblatter und des Blutes im Hiihnerei. Arch. mikr.

Anat., Bd. X, 1874. Hertwig, O., Die Lehre von den Keimblattern. Handbuch der vergl. und

exper. Entwickehuigslehre der Wirbeltiere. Vol. I. Jena, 1903. His, W., Der Keimwall des Htihnereies und die Entstehung der para blastischen Zellen. Arch. Anat. und Entw., Bd. I, 1876.

Neue Untersuchung liber die Bildung des Hiihnerembryo. Arch.

Anat. und Entw., 1877.

Lecithoblast und Angioblast der "Wirbelthiere. Histogenetische

Studien. Abh. der math.-phys. Klasse der Konigl. Sachs. Ges. der

Wissenschaften, Bd. XXVI. Leipzig, 1900.

Die Bildung der Somatopleura und der Gefasse beim Hiihnchen.

Anat. Anz., Bd. XXI, 1902. Hubbard, M. E., Some Experiments on the Order of Succession of the

Somites of the Chick. Am. Nat., Vol. 42, pp. 466-471, 1908. Janosik, J., Beitrag zur Kenntnis des Keimwulstes bei Vogeln. Sitz-Ber Akad. Wiss. Wien, math.-phys. KL, Bd. LXXXIV, 1882. Roller, C, Beitrage zur Kenntnis des Hiihnerkeimes im Beginne der Be briitung. Sitzungsber. Wien. Akad. Wiss., math.-nat. KL, 1879. Untersuchungen liber die Blatterbildung im Hlihnerkeim. Arch.

mikr. Anat., Bd. XX, 1881. V. Kolliker, a., Zur Entwickelung der Keimblatter im Hiihnerei. Verb.

phys.-med. Ges. Wlirzburg, Bd. VIII, 1875. KopscH,FR.,Ueber die Bedeutung des Primitivstreifens beim Hiihnerembryo,

und liber die ihm homologen Theile bei den Embryonen der niederen

Wirbeltiere. Intern. Monatschr. f. Anat. u. Phys., Bd. XIX, 1902. MiTROPHANOW, P. J., Teratogene Studien. II. Experimentellen Beo bachtungen liber die erste Anlage der Primitivrinne der Vogel. Arch.

Entw.-mech., Bd. VI, 1898.

Beobachtungen liber die erste Entwickelung der Vogel. Anat.

Hefte, Bd. XII, 1899. Now^\cK, K., Neue Untersuchungen liber die Bildung der beiden primiiren

Keimblatter und die Entstehung des Primitivstreifen beim Hiihnerembryo. Inaug. Diss. Berlin, 1902. Patterson, J. Thos., The Order of Appearance of the Anterior Somites in

the Chick. Biol. Bull., Vol. XIII, 1907. Patterson, J. T. An experimental Study on the Development of the Vascular

Area of the Chick Blastoderm. Biol. Bull. XVI, pp. 83-90, 1909. Peebles, Florence. Some Experiments on the Primitive Streak of the

Chick. Arch. Entw.-mech., Bd. VII, 1898.

A Prehminary Note on the Position of the Primitive Streak and its

Relation to the Embryo of the Chick. Biol. Bull., Vol. IV, 1903.


APPENDIX 447

Peebles, Florence, The Location of the Chick Embryo upon the Blastoderm. Journ. Exp. Zool., Vol. I, 1904. Platt, J. B., Studies on the Primitive Axial Segmentation of the Chick.

Bull. Mus. Comp. Zool. Harv., Vol. 17, 1889. Rabl, C, Theorie des Mesoderms. Morph. Jahrb., Bde. XV und XIX,

1889 and 1892. Rauber, a., Primitivstreifen und Neurula der Wirbelthiere, in normaler

und pathologischer Beziehung. Leipzig, 1877.

Ueber die embryonale Anlage des Hiihnchens. Centralb. d. med.

Wiss., Bd. XII, 1875.

Ueber die erste Entwickelung der Vogel und die Bedeutung der Primi tivrinne. Sitz.-ber. d. naturf. Ges. zu Leipzig, 1876. Rex, Hugo, Ueber das Mesoderm des Vorderkopfes der Ente. Archiv.

■ mikr. Anat., Bd. L., 1897. RiiCKERT, J., Entwickelung der extra-embryonalen Gefasse der Vogel. Hand buch der vergl. w. exp. Entw.-lehre der Wirbelthiere, Bd. I, T. 1,

1906.

Ueber die Abstammung der bluthaltigen Gefassanlagen beim Huhn,

und uber die Entstehung des Randsinus beim Huhn und bei Torpedo.

Sitzungsber. der Bay. Akad. Wiss., 1903. ScHAUiNSLAND, H., Bcitrage zur Biologie und Entwickelung der Hatteria

nebst Bemerkungen uber die Entwickelung der Sauropsiden. Anat.

Anz. XV, 1899. ViALLETOX, Developpement des aortes chez I'embryon de poulet. Journ.

de I'^nat. T. XXVIII, 1892. See also Anat. Anz., Bd. VII, 1892. ViRCHOW, H., Der Dottersack des Huhns. Internat. Beitrage zur wiss.

Med., Bd. I, 1891. Waldeyer, W., Bemerkungen uber die Keimblatter und den Primitivstreifen

bei der Entwickelung des Huhnerembryo. Zeitschr. rationeller Medicin,

1869. Whitman, C. O., A Rare Form of the Blastoderm of the Chick and its Bearing

on the Question of the Formation of the Vertebrate Embryo. Quar.

Journ. Micr. Sc, Vol. XXIII, 1883. WiLLL\MS, Leonard W. The Somites of the Chick. Am. Journ. of Anat.,

Vol. 11, pp. 5.5-100, 1910.

Literature to Chapter VI included in following chapters.

LITERATURE — CHAPTER VII

CHARBONNEiy-SALLE ct Phisalix, De I'evolution postembryonnaire du

sac vitellin chez les oiseaux. C. R. Acad. Sc, Paris, 1886. Dareste, C, Sur I'absence totale de I'amnios dans les embryons de poule.

C. R. Acad. Sc, Paris, T. LXXXVIII, 1879. Duval, M., Etudes histologiques et morphologiques sur les annexes des

embryons d'oiseau. Journ. de I'anat, et de la phys., T. XX, 1884. Etude sur I'origine de Tallantoide chez le poulet. Rev. sc. nat.,

Paris, 1877.


448 APPENDIX

Duval, M., Sur ime organe placentoide chez rembryon des oiseaux. C. R.

Acad. Sc, Paris, 1884. Fromann, C, Ueber die Struktur der Dotterhaut des Huhnes. Sitz.-ber.

Jen. Ges. Medizin u. Naturw., 1879. FuLLEBORN, F., Beitrage zur Entwickelung der Allantois der Vogel. Diss.,

Berlin, 1894. Gasser, E., Beitrage zur Entwickelungsgeschichte der Allantois, der Miiller schen Gange iind des Afters. Frankfurt a. M., 1874. GoTTE, A., Beitrage zur Entwickelungsgeschichte des Darmkanals im Hiihn chen. Tubingen, 1867. HiROTA, S., On the Sero-amniotic Connection and the Foetal Membranes in

the Chick. Journ. Coll. Sc. Imp. Univ. Japan, Vol. VI, Part IV, 1^94. LiLLiE, Frank R., Experimental Studies on the Development of the Organs

in the Embryo of the Fowl (Gallus domesticus): 1. Experiments on the

Amnion and the Production of Anamniote Embryos of the Chick. Biol.

Bull., Vol. V, 1903. 2. The Development of Defective Embryos and

the Power of Regeneration. Biol. Bull., Vol. VII, 1904. Mertens, H., Beitrage zur Kenntniss der Fotushiillen im Vogelei. Meckels

Archiv, 1830. Mitrophanow, p. J., Note sur la structure et la formation de I'enveloppe

du jaune de I'ceuf de la poule. Bibliogr. Anat., Paris, 1898. PopoFF, Demetrius, Die Dottersackgefasse des Huhnes. Wiesbaden, 1894. Pott, R., and Preyer, W., Ueber denGaswechsel und die chemischen Verander ungen des Hiihnereies wahrend der Bebriitung. Archiv. ges. Phys., 1882. Preyer, W., Specielle Physiologic des Embryo. Leipzig, 1885. Ravn, E., Ueber die mesodermfreie Stelle in der Keimscheibe des Huhner embryo. Arch. Anat. u. Entw., 1886.

Ueber den Allantoisstiel des Hiihnerembryo. Verh. Anat. Ges., 1898. ScHAUiNSLAND, H., Die Entwickelung der Eihaute der Reptilien und der

Vogel. Handbuch der vergl. und exp. Entw.-lehre der Wirbeltiere. Bd.

I, T. 2, 1902.

Beitrage zur Entwickelungsgeschichte der Wirbeltiere. II. Beitrage zur

Entwickelungsgeschichte der Eihaute der Sauropsiden. Bibliotheca

Zoologica, 1903. Schenk, S. L., Beitrage zur Lehre vom Amnion. Archiv. mikr. Anat., Bd.

VII, 1871.

Ueber die Aufnahme des Nahrungsdotters wahrend des Embryonal lebens. Sitz.-ber. Akad. Wiss. Wien, math.-nat. Kl., 1897. Shore, T. W., and Pickering, J. W., The Proamnion and Amnion in the

Chick. Journ. of Anat. and Phys., Vol. XXIV, 1889. Soboleff, Die Verletzung des Amnions wahrend der Bebriitung. Mittheil,

embryolog. Inst., Wien, 1883. Strahl, H., Eihaute und Placenta der Sauropsiden. Ergeb. Anat. u. Entw. gesch., Bd. I, 1891. Stuart, T. P. A., A Mode of Demonstrating the Developing Membranes in

the Chick. Journ. Anat. and Phys., London, Vol. XXV, 1899. ViRCHOW, H., Beobachtungen am Hiihnerei; iiber das dritte Keimblatt

im Bereiche des Dottersackes. Virchow's Arch., Bd. LXII, 1874.


APPENDIX 449

ViRCHOW, H., Ueber das Epithel des Dottersackes im Hiihnerei. Diss., Berlin. 1875.

Der Dottersack des Huhnes. Internat. Beitrage zur wissenschaft. Medizin, Bd. I, 1891.

Das Dotterorgan der Wirbeltiere. Zeitschr. wiss. Zool., Bd. LIII, Suppl., 1892.

Das Dotterorgan der Wirbelthiere. Arch. mikr. Anat., Bd. XL, 1892. Dottersyncytium, Keimhautrand und Beziehungen zur Koncrescenzlehre. Ergeb. Anat. u. Entw., Bd. VI, 1897.

Ueber Entwickelungsvorgange, welche sich in den letzten Bruttagen am Hiihnerei abspielen. Anat. Anz., Bd. IV, BerHn, 1889. VuLPiAX, La physiologie de I'amnios et de I'allantoide chez les oiseaux.

Mem. soc. biol., Paris, 1858. Weldox, W. F. R., Prof, de Vries on the Origin of Species. (Includes experiments on amnion.) Biometrica, Vol. I, 1902.

LITERATURE — CHAPTER VIII

Beard, J., Morphological Studies, II. The Development of the Peripheral

Nervous System of Vertebrates. Pt. I. Elasmobranchs and Aves.

Quar. Journ. Micr. Sc, Vol. XXIX, 1888. Beraneck, E., Etudes sur les replis medullaires du poulet. Recueil Zool.

Suisse, Vol. IV, 1887. Bethe, Albrecht, Allgemeine Anatomic und Physiologie des Nervensys tems. Leipzig, 1903. Brandis, F., Untersuchungen iiber das Gehirn der Vogel. Arch. mikr.

Anat., Bd. XLI, 1893; Bd. XLIII, 1894; Bd. XLIV, 1895. Burrows, Montrose T., The Growth of Tissues of the Chick Embryo

Outside the Animal Body, with Special Reference to the Nervous System.

Journ. Exp. Zoology, Vol. 10, pp. 63-83, 1911. Cajal, S. R. y., Sur I'origine et les ramifications des fibres nerveuses de la

moelle embryonnaire. Anat. Anz., Bd. V, 1890.

A quelle epoque aparaissent les expansions des cellules nerveuses de

la moelle epiniere du poulet. Anat. Anz., Bd. V, 1890. Froriep, a., Ueber Anlagen von Sinnesorganen am Facialis, Glossopha ryngeus und Vagus, iiber die genetische Stellung des Vagus zum Hypo glossus, und iiber die Herkunft der Zungenmuskulatur. Arch. Anat.

u. Entw., 1885. Carpenter, Frederick Walton, The Development of the Oculomotor Nerve,

the Ciliary Ganglion, and the Abducent Nerve in the Chick. Bull.

Mus. Comp. Zool. Harv. Vol. XLVIII, 1906. DissE, J., Die erste Entwickelung des Riechnerven. Anat. Hefte, Abth. I,

Bd. IX, 1897. GoLoviNE, E., Sur le developpement du systeme ganglionnaire chez le poulet.

Anat. Anz., Bd. V, 1890. GoRONOwiTscH, N., Die axiale und die laterale (A. Goette) Kopfmetamerie

der Vogeleml^ryonen. Anat. Anz., Bd. VII, 1892.

L'ntersuchungen iiber die Entwickelung der Sogenannten " Ganglien leisten " im Kopfe der Vogelembryonen. Morph. Jahrb., Bd. XX, 1893.


450 APPENDIX

Heinrich, Georg, Untersuchungen iiber die Anlage des Grosshirns beim Hiihnchen. Sitz.-ber. d. Ges. f. Morph. u. Phys. in Munchen, Bd. XII,

1897. Hill, Charles, Developmental History of the Primary Segments of the

Vertebrate Head. Zool. Jahrbucher, Abth. Anat. Bd. XIII, 1900. His, W., Die Neuroblasten und deren Entstehung im embryonalen Mark.

Abh. math.-physik. Klasse, Konigl. Sachs. Ges. Wiss., Bd. XV, 1889. Histogenese und Zusammenhang der Nervenelemente. Arch. Anat. u. Entw., Suppl., 1890. Ueber das frontale Ende des Gehirnrohres. Arch. Anat. u. Entw., 1893. Ueber das frontale Ende und iiber die natiirliche Eintheilung des Gehirnrohres. Verh. anat. Ges., Bd. VII, 1893. His, W. (Jr.)» Ueber die Entwickelung des Bauchsympathicus beim Hiihnchen und Menschen. Arch. Anat. u. Entw., Suppl., 1897. V. KoLLiKER, Ueber die erste Entwickelung der Nervi olfactorii. Sitz.-ber.

phys. med. Ges. zu Wiirzburg, 1890. V. KuPFFER, K., Die Morphogenie des Centralnervensystems. Handbuch der

vergl. und exp. Entwickelungslehre der Wirbeltiere, Kap. VIII, IP, 1905. Lewis, M. R. and Lewis, W. H., The Cultivation of Tissues from Chick

Embroyos in Solutions of NaCl, CaCl2, KCl and NaHCOg. Anatomical

Record, Vol. 5, pp. 277-293. See also Anat. Rec, Vol. 6, nos. 1 and 5, 1911. Marshall, A. M., The Development of the Cranial Nerves in the Chick.

Quar. Journ. Micr. Sc, Vol. XVIII, 1878.

The Segmental Value of the Cranial Nerves. Journ. Anat. and Physiol.,

Vol. XVI, 1882. v. MiHALCOVics, v., Entwickelungsgeschichte des Gehirns. Leipzig, 1877. Onodi, a. D., Ueber die Entwickelung des sympathischen Nervensy stems.

Arch. mikr. Anat., Bd. XXVI, 1886. Rabl, C, Ueber die IMetamerie des Wirbelthierkopfes. Verh. anat. Ges.,

VI, 1892. RuBASCHKiN, W., Ueber die Beziehungen des Nervus trigeminus zur Riech schleimhaut. Anat. Anz., Bd. XXII, 1903. Weber, A., Contribution a Tetude de la metamerism du cerveau anterieur

chez quelques oiseaux. Arch, d'anat. microsc, Paris, T. Ill, 1900. Van Wijhe, J. W., L^eber Somiten und Nerven im Kopfe von Vogel- und

Reptilien-embryonen. Zool. Anz. Bd. IX, 1886.

Ueber die Kopfsegmente und das Geruchsorgan der Wirbelthiere

Zool. Anz., Bd. IX, 1886.

LITERATURE — CHAPTER IX Organs of Special Sense

A. The Eye

Addario, C, Sulla struttura del vitreo embryonale e de' neonati, sulla matrice del vitreo e suU' origine della zonula. Ann. OttalmoL, Anno 30, 1901-1902.


APPENDIX 451

AddariOjC, Ueber die Matrix desGlaskorpers im menschlichen und thierischen

Auge. Vorlauf. Mitth. Anat. Anz., Bd. XXI, 19(32. Agababow, Untersuchiingen iiber die Natur der Zonula ciliaris. Arch.

mikr. Anat., Bd. L, 1897. Angelucci, a., Ueber Entwiekelung und Bau des vorderen Uvealtractus der

Vertebraten. Arch. mikr. Anat., Bd. XIX, 1881. Arnold, J., Beitrage zur Entwickekmgsgeschichte des Auges. Heidelberg,

1874. AssHETON, R., On the Development of the Optic Nerve of Vertebrates, and

the Choroidal Fissure of Embryonic Life. Quar. Journ. Micr. Sc, Vol.

XXXIV, 1892. Bernd, Adolph Hugo, Die Entwiekelung des Pecten im Auge des Hiihn chens aus den Blattern der Augenblase. Bonn, 1905. Cajal, S. R. y., Sur la morphologie et les connexions des elements de la retine

des oiseaux. Anat. Anz. Bd. IV, 1889.

Sur la fine structure du lobe optique des oiseaux et sur I'origine reelle

des nerfs optiques. Int. Monatschr. Anat. u. Phys., Bd. VIII, 1891. Cirincione, G., Ueber die Entwiekelung der Capsula perilenticularis. Arch.

Anat. u. Entw., Suppl. Bd., Jahrg. 1897.

Zur Entwiekelung des Wirbeltierauges. Ueber die Entwiekelung

des Capsula perilenticularis. Leipzig, 1898.

Ueber die Genese des Glaskorpers bei Wirbelthieren. Verh. Anat.

Ges., 17. Versamml. in Heidelberg, 1903. Collin, R., Recherches sur le developpement du muscle sphincter de I'iris

chez les oiseaux. Bibliog. Anat., T. XII, fasc. V. Paris, 1903. Froriep, a., Ueber die Entwiekelung des Sehnerven. Anat. Anz., Bd. VI,

1891.

Die Entwiekelung des Auges der Wirbeltiere. Handb. der vergl. u.

exp. Entw.-l. der Wirbeltiere, Bd. II, 1905. HuscHKE, E., Lieber die erste Entwiekelung des Auges und die damit zusam menhangende Cyklopie. Meckel's Arch., 1832. Kessler, L., Untersuchungen liber die Entwiekelung des Auges, angestellt

am Hiihnchen und Tauben. Dissertation. Dorpat, 1871.

Die Entwiekelung des Auges der Wirbelthiere. Leipzig, 1877. V. Kolliker, a., LTeber die Entwiekelung und Bedeutung des Glaskorpers.

Verh. anat. Ges., 17. Vers. Heidelberg, 1903.

Die Entwiekelung und Bedeutung des Glaskorpers. Zeitschr. wiss.

Zool., Bd. LXXVII, 1904. V. Lenhossek, M., Die Entwiekelung des Glaskorpers. Leipzig, 1903. Lewis, W. H., Wandering Pigmented Cells Arising from the Epithelium of

the Optic Cup, with Observations on the Origin of the M. Sphincter

Pupillffi in the Chick. Am. Journ. Anat., Vol. II, 1903. LocY, W. A., Contribution to the Structure and Development of the Vertebrate Head. Journ. Morph., Vol. XI. Boston, 1895.

Accessory Optic Vesicles in the Chick Embryo. Anat. Anz., Bd. XIV,

1897. NussBAUM, M., Zur Riickbildung embryonaler Anlagen. (Corneal papillae

of chick embryos.) Archiv. mikr. Anat., Bd. LVII, 1901.


452 APPENDIX

NussBAUM, M., Die Pars ciliaris retinae des Vogelauges. Arch. mikr. Anat., Bd.

LVII, 1901.

Die Entwiekelung der Binnenmuskeln des Aiiges der Wirbeltiere.

Arch. mikr. Anat., Bd. LVIII, 1901. Rabl, C, Ziir Frage nach der Entwickehmg des Glaskorpers. Anat. Anz.,

Bd. XXII, 1903.

Ueber den Ban und die Entwickehmg der Linse. II. Reptihen imd

Vogel. Zeitschr. wiss. Zool., Bd. LXV, 1899. Robinson, A., On the Formation and Structure of the Optic Nerve, and its

Relation to the Optic Stalk. Journ. Anat. and Phys. London, 1896. SziLi, A.V. Beitrag zur Kenntniss der Anatomic und Entwickelungsgeschichte

der hinteren Irisschichten, etc. Arch. Opthalm., Bd. LIII, 1902.

Zur Anatomic und Entwickelungsgeschichte der hinteren Irisschichten, etc. Anat. Anz., Bd. XX, 1901.

Zur Glaskorperfrage. Anat. Anz. Bd. XXIV, 1904. ToRNATOLA, Origiuc et nature du corps vitre. Rev. gener. d 'opthalm. Annee

14, 1897. UcKE, A., Epithelreste am Opticus und auf der Retina. Arch. mikr. Anat.,

Bd. XXXVIII, 1891.

Zur Entw^ickelung des Pigmentepithels der Retina. Diss, aus Dorpat.

Petersburg, 1 89 1 . ViRCHOW, H., Facher, Zapfen, Leiste, Polster, Gefasse im Glaskorperraum

von Wirbelthieren, sowie damit in Verbindung stehenden Fragen. Er gebn. Anat. u. Entw., Bd. X. Berlin, 1900. Weysse, a. W., and Burgess, W. S., Histogenesis of the Retina. Am.

Naturalist, Vol. XL, 1906.


B. The Nose

Born, G., Die Nasenhohlen und der Thranennasengang der amnioten Wir belthiere II. Morph. Jahrb., Bd. V, 1879; Bd. VIII, 1883. CoHN, Franz, Zur Entwickelungsgeschichte des Geruchsorgans des Hiihn chens. Arch. mikr. Anat., Bd. LXI, 1903. Dieulafe, Leon, Les fosses nasales des vertebres (morphologic et embry ologie). Journ. de I'anat. et de la phys., T. 40 and 41, 1904 and 1905.

(Translated by Hanau W. Loeb: Ann. of Otol., Rhin. and Laryng., Mar.,

June and Sept., 1900.) Disse, J., Die erste Entwiekelung des Riechnerven. Anat. Hefte, Bd. IX,

1897. Ganin, M., Einige Thatsachen zur Frage iiber das Jacobsohn'sche Organ der

Vogel. Arb. d. naturf. Ges. Charkoff, 1890 (russisch). Abstr. Zool.

Anz., 1890. V. KoLLiKER, A., Ueber die Entwickehmg der Geruchsorgane beim Menschen

und Hiihnchen. Wiirzburger med. Zeitschr., Bd. I, 1860. V. MiHALKOvics, v., Nasenhohle und Jacobson'sche Organ. Anat. Hefte,

I. Abth., Bd. XI, 1898. Peter, Karl, Entwickehmg des Geruchsorgans und Jakobson'sche Organs

in der Reihe der Wirbeltiere. Bildung der ausseren Nase und des


APPENDIX 453

Gaumens. Handbuch der vergl, und experiment. Entwickelimgslehre

der Wirbeltiere. IP, 1902. Preobraschensky, L., Beitrage zur Lehre liber die Entwiekelung des Ge ruchsorganes des Huhnes. Mitth. embryol. Inst. Wien, 1892. PuTELLi, F., Ueber das Verhalten der Zellen der Riechschleimhaut bei

Hiihnerembryonen friiher Stadien. Mitth. embr. Inst. Wien, 1889.

C. The Ear

Hasse, C, Beitrage zur Entwiekelung der Gewebe der hautigen Vogel schnecke. Zeitschr. wiss. Zool., Bd. XVII, 1867. HuscHKE, Ueber die erste Bildungsgeschichte des Auges und Ohres beim

bebriiteten Hiihnchen. Isis von Oken, 1831. Kastschenko, N., Das Schlundspaltengebiet des Hiihnchens. Arch. Anat.

u. Entw., 1887. Keibel, Ueber die erste Bildung des Labyrinthanhanges. Anat. Anz., Bd.

XVI, 1899. Krause, R., Die Entwickekmg des Aquaeductus Vestibuh, s. Ductus endo lymphaticus. Anat. Anz., Bd. XIX, 1901.

Die Entwickekmgsgeschichte des hautigen Bogenganges. Arch. mikr.

Anat., Bd. XXXV, 1890. MoLDENHAUER, W., Die Entwickcking des mittleren und des ausseren Ohres.

Morph. Jahrb., Bd. Ill, 1877. PoLi, C, Sviluppo della vesicula auditiva; studio morphologico. Genoa,

1896.

Zur Entwickekmg der Gehorblase bei den WirbeUieren. Arch. mikr.

Anat., Bd. XLVIII, 1897. Retzius, G., Das Gehororgan der Wirbelthiere. II. Theil, Reptihen Vogel,

Sanger. Stockhokn. 1881-1884. RoTHiG, p., und Brugsch, Theodor, Die Entwickekmg des Labyrintkes

beim Huhn. Archiv. mikr. Anat., Bd. LIX, 1902. RtJDiNGER, Zur Entwickekmg des hautigen Bogenganges des inneren Ohres.

Sitzungsber. Akad. Miinchen, 1888.

LITERATURE — CHAPTER X The Alimentary Tract and Its Appendages

A. The Oral Cavity and Organs

Fraisse, p., Ueber Zahne bei Vogeln. Vortrag, geh. in der phys.-med.

Ges. Wiirzburg, 1880. Gardiner, E. G., Beitrage zur Kenntniss des Epitrichiums und der Bikkmg

des Vogelscknabels. Inaug. Dissert. Leipzig, 1884. Arch. mikr. Anat., Bd. XXIV, 1884. Gauff, E., Anat. L^ntersuchungen iiber die Nervenversorgung der Mund und Nasenhohledrusen der Wirbekiere. Morph. Jahrb., Bd. XIV, 1888. GiACOMiNi, E., Sulle glanduH sakvari degk uccelk. Richerche anatomico embrologiche. Monit. zook Itak, Anno 1, 1890.


454 APPENDIX

GoppERT, E., Die Bedeutimg der Zunge ftir den secundaren Gaumen und den

Ductus naso-pharyngeus. Beobachtungen an Reptilien und Vogeln.

Morph. Jahrb., Bd. XXXI, 1903. Kallius, E., Die mediane Thyreoideaanlage und ihre Beziehung zum Tuber culum impar. Verb. anat. Ges., 17. Vers., 1903.

Beitrage zur Entwickelung der Zunge. Verb. anat. Ges., 15. Vers.

Bonn, 1901. Manno, Andrea, Sopra il niodo onde si perfora e scompare le membrana

faringea negli embrioni di polio. Richerche Lab. Anat. Roma, Vol.

IX, 1902. Oppel, a., Lehrbuch der vergleichenden mikroskopischen Anat. der Wir beltiere. Jena, 1900. Reichel, p., Beitrag zur Morphologie der ^Mundhohlendriisen der Wirbel thiere. Morph. Jahrb., Bd. VIII, 1883. Rose, C., Ueber die Zahnleiste und die Eischwiele der Sauropsiden. Anat.

Anz., Bd. VII, 1892. Sluiter, C. p., Ueber den Eizahn und die Eischwiele einiger Reptilien.

Morph. Jahrb., Bd. XX, 1893. Yarrell, W., On the Small Horny Appendage to the Upper Mandible in

Very Young Chickens. Zool. Journal, 1826.

B. Derivatives of the Emhryonic Pharynx

van Bemmelen, J. F., Die Visceraltaschen und Aortenbogen bei Reptilien

und Vogeln. Zool. Anz., 1886. His, W., Ueber den Sinus praecervicalis und die Thymusanlage. Arch.

Anat. u. Entw., 1886.

Schlundspalten und Thymusanlage. Arch. Anat. u. Entw., 1889. Der Tractus Thyreoglossus und seine Beziehung zum Zungenbein.

Arch. Anat. u. Entw., 1891. Kastschenko, N., Das Schlundspaltengebiet des Hiihnchens. Arch. Anat.

und Entw., 1887. LiESSNER, E., Ein Beitrag zur Kenntniss der Kiemenspalten und ihrer An lagen bei amnioten Wirbelthieren. Morph. Jahrb., Bd. XIII, 1888. Mall, F. P., Entwickelung der Branchialbogen und Spalten des Hiihnchens.

Arch. Anat. und Entw., 1887. DE Meuron, p., Recherches sur le developpement du thymus et de la glande

thyreoide. Dissertation, Geneve, 1886. MiJLLER, W., Ueber die Entwickelung der Schilddriise. Jen. Zeitschr., Bd.

VI, 1871. Seessel, a., Zur Entwickelungsgeschichte des Vorderdarms. Arch. Anat.

und Entw., 1877. Verdun, M. P., Sur les derives branchiaux du poulet. Comptes rendus

Soc. Biol., Tom. V. Paris, 1898.

Derives branchiaux chez les vertebres superieurs. Toulouse, 1898.


APPENDIX 455

C. (Esophagus, Stomach, Intestine

BoRNHAUPT, Th., Uritersuchiingen fiber die Entwickelung des Urogenital systems beim Huhnchen. Inaug. Diss. Riga, 1867. Cattaneo, G., Intorno a un recente lavoro sullo stomaco degli iiccelli. Pavia,

1888.

Istologia e sviluppo del apparato gastrico degli uceelli. Atti della

Soc. Ital. di Sc. Nat., Vol. XXVII, Anno 1884. Milano, 1885. Cazin, M., Recherches anatomiques, histologiques et embryologiques sur

I'appareil gastrique des oiseaux. Ann. Sc. Xat. Zool. 7 ser., Tom. IV,

1888.

Sur le developpement embryonnaire de Testomac des oiseaux. Bull.

de la societe philomathique de Paris. 7 ser., Tom. XI, Paris, 1887. Developpement de la couehe cornee du gesier du poulet et des glandes

qui la seeretent. Comptes rendus, T. CI, 1885. Cloetta, M., Beit rage zur mikroskopischen Anatomic des Vogeldarmes.

Archiv. mikr. Anat., Bd. XLI, 1893. Fleischmaxx, Albert, Morphologische studien uber Kloake und Phallus der

Amnioten. III. Die Vogel, von Dr. Carl Pomayer. Morph. Jahrb.,

Bel. XXX, 1902. Gasser, E., Beitrage zur Entwiekelungsgeschichte der Allantois, Miiller schen Gauge und des Afters. Frankfurt a. M., 1893.

Die Entstehung der Kloakenoffnung bei Hiihnerembryonen. Arch.

Anat. u. Entw., 1880. Maurer, F., Die Entwickelung des Darmsystems. Handb. d. vergl. u.

exp. Entw.-lehre der Wirbeltiere. 11^, 1902. v. MiHALCovics, v., Untersuchungen liber die Entwickelung des Harn- und

Geschlechtsapparates der Amnioten. Internat. Monatschr. Anat. u.

Phys., Bd. II, 1885-1886. MiNOT, C. S., On the Solid Stage of the Large Intestine in the Chick. Journ.

Bos. Soc. Med. Sc, Vol. IV, 1900. Pomayer, Carl. See Fleischmann. Retterer, E., Contributions a I'etude du cloaque et de la bourse de Fabricius

chez des oiseaux. Journ. de I'anat. et de la phys. 21 An. Paris, 1885. Seyfert, Beitrage zur mikroskopischen Anatomic und zur Entwiekelungsgeschichte der blinden Anhange des Darmcanals bei Kaninchen, Taube

unci Sperling. Inaug. Diss. Leipzig, 1887. ScHW^\RZ, D., Untersuchungen des Schwanzendes bei den Embryonen der

Wirbeltiere. Zeitschr. wiss. Zool., Bd. XL VIII, 1889. Stieda, L. LudwiG, L^eber den Bau und die Entwickelung der Bursa Fabricii.

Zeitschr. wiss. Zool., Bd. XXXIV, 1880. Swenander, G., Beitrage zur Kenntniss des Kropfes der Vogel. Zool. Anz.,

Bd. XXIT, 1899. Weber, A., Quelques faits concernant le developpement de Tintestin moyen,

et de ses glandes annexes chez les oiseaux. C. R. Soc. Biol., T. LIV. Paris,

1902. Wenckebach, K. F., De Ontwikkeling en de bouw der Bursa Fabricii. Inaug. Dissert. Leiden, 1888.


456 APPENDIX

D. Liver and Pancreas

Bracket, A., Die Entwickelung unci Histogenese der Leber und des Pancreas.

Ergebnisse d. Anat. u. Entw.-gesch., 1896. Brouha, M., Recherches sur le developpement du foie, du pancreas, de la

cloison mesenterique et des cavites hepato-enteriques chez les oiseaux.

Journ. de Tanat. et phys., T. XXXIV. Paris, 1898.

Sur les premieres phases du foie et sur revolution des pancreas ven traux chez les oiseaux. Anat. Anz., Bd. XIV, 1898. Choronschitzky, B., Die Entstehung der Milz, Leber, Gallenblase, Bauch speicheldriise und des Pfortadersystems bei den verschiedenen Abthei lungen der Wirbelthiere. Anat. Hefte, Bd. XIII, 1900. Felix, W., Zur Leber und Pancreasentwickelung. Arch. Anat. u. Entw., 1892. Frobeen, F., Zur Entwickelung der Vogelleber. Anat. Hefte, 1892. GoTTE, Alex., Beitrage zur Entwickelungsgeschichte des Darmcanals im

Huhnchen. Tubingen, 1867. Hammar, G. a., Ueber Duplicitat ventraler Pancreasanlage. Anat. Anz.,

Bd. XIII, 1897.

Ueber einige Hauptztige der ersten embryonalen Leberentwickelung.

Anat. Anz., Bd. XIII, 1897.

Einige Plattenmodelle zur Beleuchtung der fruheren embryonalen

Leberentwickelung. Arch. Anat. u. Entw., 1893. MiNOT, C. S., On a Hitherto Unrecognized Form of Blood-Circulation without

Capillaries in the Organs of Vertebrata. Proc. Boston Soc. of Nat.

Hist., Vol. XXIX, 1900. ScHREiNER, K. E., Beitrage zur Histologic und Embryologie des Vorder darms der Vogel. Zeitschr. wiss. ZooL, Bd. LXVIII, 1900. Shore, T. W., The Origin of the Liver, Journ. of Anat. and Phys., Vol. XXV,

1890-91. Saint-Remy, Sur le developpement du pancreas chez les oiseaux. Rev.

biol. du Nord de la France. Annee V, 1893.

E. The Respiratory Tract

Bar, M., Beitrage zur Kenntniss der Anatomic und Physiologic der Athemwerkzeuge bei den Vogeln. Zeitschr. wiss. Zool., Bd. LXI, 1896.

Bertelli, D., Sviluppo de sacchi aeriferi del polio. Divisione della cavita celomatica degli uccelli. Atti della Societa Toscana di scienze natural! residente in Pisa. Memorie, Vol. XVII, 1899.

Blumsteix-Judina, Beila, Die Pneumatisation des Markes der Vogelknochen. Anat. Hefte, Abth. I, Bd. XXIX (Heft 87), 1905.

Camp ANA, Recherches d 'anatomic de physiologic, et d 'organogenic pour la determination des lois de la genese et de revolution des especes animals. I. Memoire. Physiologic de la respiration chez les oiseaux. Anatomic de I'appareil pneumatique puhnonnaire, des faux diaphragmes, des seremus et de I'intestin chez le poulet. Paris, Masson, 1875.

Goeppert, E., Die Entwickelung der luftfiihrenden Anhange des Vorderdarms. Handbuch d. vergl. u. exp. Entw.-lehre der Wirbeltiere, Bd. II, T. 1, 1902.


APPENDIX 457

LocY, W. A. and Larsell, O., The Embryology of the Bird's Lung, Based on Observations of the Domestic Fowl. Am. Journ. of Anat., Vol. 19, pp. 447-504, and Vol. 20, pp. 1-44, 1916.

Rathke, M. H., Ueber die Entwickelung der Atemwerkzeuge bei den Vogeln und Saugetieren. Nov. Act. Acad. Caes. Leop. Car., T. XIV. Bonn, 1828.

Selenka, E., Beitrage zur Entwickelungsgeschichte der Luftsiicke des Huhnes. Zeitschr. wiss. Zool., Bd. XVI, 1866.

Strasser, H., Die Luftsacke der Vogel. Morph. Jahrb., Bd. Ill, 1877.

Weber, A., et Buvignier, A., Les premieres phases du developpement du poumon chez les embryons de poulet. Comptes rendus hebd. des seances de la societe de Biologie, Vol. LV. Paris, 1903.

WuNDERLiCH, L., Beitrage zur vergleichenden Anatomie und Entwickelungsgeschichte des unteren Kehlkopfes der Vogel. Nova Acta Acad. Caes. Leop. Carol. Germanicae, Bd. XL VIII, 1884.


LITERATURE — CHAPTER XI

Beddard, F. E., On the Oblique Septa ("Diaphragm" of Owen) in the Passerines and some other Birds. Proc. Zool. Soc. London, 1896.

Bertelli, D., Sullo sviluppo del diaframma dorsale nel Polio. Nota preventiva. Monit. Zool. Ital., Anno IX, 1898.

Contributo alia morfologia ed alio sviluppo del diaframma ornitico. Ibid., 1898.

Bracket, A., Die Entwickelung der grossen Korperhohlen imd ihre Trennung von einander, etc. Ergebnisse d. Anat. u. Entw.-gesch., Bd. VII, 1897.

Broman, Ivar, Die Entwickelungsgeschichte der Bursa omentalis und ahnlicher Recessbildungen bei den Wirbeltieren. Wiesbaden, 1904.

B-ROUHA, M. See Chap. X.

Butler, G. W., On the Subdivision of the Body Cavity in Lizards, Crocodiles and Birds. Proc. Zool. Soc. London, 1889.

Choronschitzky, B. See Chap. X.

Dareste, C, Sur la formation du mesentere et de la gouttiere intestinale dans Tembryon de la poule. Comptes rendus, T. CXII, 1891.

HocHSTETTER, F., Die Entwickelung des Blutgefasssystems. Handbuch der vergl. und exp. Entw.-lehre der Wirbeltiere. IIP, 1903.

Janosik, J., Le pancreas et la rate. Bibliographic Anat. Annee 3. Paris, 1895.

LocKWOOD, C. B., The Early Development of the Pericardium, Diaphragm and Great Veins. Phil. Trans. Roy. Soc, London, Vol. CLXXIX, 1889.

Mall, F. P., Development of the Lesser Peritoneal Cavity in Birds and Mammals. Journ. Morph., Vol. V, 1891.

Maurer, F., Die Entwickehmg des Darmsystems. Handbuch d. vergl. u. exp. Entw.-lehre d. Wirbeltiere, Vol. II, 1906.

Peremeschko, LTeber die Entwickelung der Milz. Sitzungsber. d. Akad. d. Wiss. in Wien, math., naturwiss. Klasse, Bd. LVI, Abth. 2, 1867.

Ravn, E., Die Bildung des Septum transversum beim Hiihnerembryo. Arch. Anat. u. Entw., 1896. See also Anat. Anz., Bd. XV, 1899.


458 APPENDIX

Reichert, Entwickelungsleben im Wirbeltierreich. Berlin, 1840. Remak, Untersuchungen liber die Entwickelung des Wirbeltierreichs, p. 60,

1850-1855. UsKOW, W., Ueber die Entwickelung des Zwerchfells, des Pericardium und

des Coeloms. Arch. mikr. Anat., Bd. XXII, 1883. WoiT, O., Zur Entwickelung der Milz. Anat. Hefte, Bd. IX, 1897.

LITERATURE — CHAPTER XII

V. Baer, K. E., Ueber die Kiemen und Kiemengefasse im den Embryonen

der Wirbeltiere. Meckel's Archiv., 1827. VAN Bemmelen, J., Die Visceraltaschen und Aortenbogen bei Reptilien und

Vogeln. Zool. Anz., 1886. Boas, J. E. V., Ueber die Aortenbogen der Wirbeltiere. Morph. Jahrb.,

Bd. XIII, 1887. Brouha. See Chap. X. HocHSTETTER, F., Die Entw^ickelung des Blutgefasssystems (des Herzens

nebst Herzbeutel und Zwerchfell, der Blut- und Lymphgefasse, der

Lymphdriisen und der Milz in der Reihe der Wirbeltiere). Handbuch

der vergl. und exp. Entwickelungslehre der Wirbeltiere. IIP, 1903. Beitrage zur Entwickelungsgeschichte des Venensystems der Amnioten.

I. Hiihnchen. Morph. Jahrb., Bd. XIII, 1888.

Ueber den Ursprung der Arteria Subclavia der Vogel. Morph. Jahrb,

Bd. XVI, 1890.

Entwickelung des Venensystems der Wirbeltiere. Ergeb. der Anat.

u. Entw., Bd. Ill, 1893. HuscHKE, E., Ueber die Kiemenbogen und Kiemengefasse beim bebriiteten

Hiihnchen. Isis, Bd. XX, 1827. Langer, a., Zur Entwickelungsgeschichte des Bulbus cordis bei Vogeln und

Saugetieren. Morph. Jahrb., Bd. XXII, 1894. LiNDES, G., Ein Beitrag zur Entwickelungsgeschichte des Herzens. Dissertation. Dorpat, 1865. LocY, W. A., The Fifth and Sixth Aortic Arches in Chick Embryos with

Comments on the Condition of the Same Vessels in other Vertebrates.

Anat. Anz., Bd. XXIX, 1906. Mackay, J. Y., The Development of the Branchial Arterial Arches in Birds,

with Special Reference to the Origin of the Subclavians and Carotids.

Phil. Trans. Roy. Soc, London, Vol. CLXXIX, 1889. Masius, J., Quelques notes sur le developpement du coeur chez le poulet.

Arch. Biol., T. IX, 1889. Miller, W. S., The Development of the Postcaval Veins in Birds. Am.

Journ. Anat., Vol. II, 1903. PopoFF, D., Die Dottersackgefasse des Huhnes. Wiesbaden, 1894. Rathke, H., Bemerkungen iiber die Entstehung der bei manchen Vogeln

und den Krokodilen vorkommenden unpaaren gemeinschaftlichen Carotis.

Arch. Anat. u. Phys., 1858. Rose, C, Beitrage zur vergleichenden Anatomie des Herzens der Wirbeltiere. Morph. Jahrb., Bd. XVI, 1890.


APPENDIX 459

Rose, C, Beitrage zur Entwickelungsgeschichte des Herzens. Inaug. Dissert.

Heidelberg, 1888. ToNGE, Morris, On the Development of the Semilunar Valves of the Aorta

and Pulmonary Artery of the Chick. Phil. Trans. Roy. Soc, London,

Vol. CLIX, 1869. Twining, Granville H., The Embryonic History of the Carotid Arteries

in the Chick. Anat. Anz., Bd. XXIX, 1906. ViALLETON, L., Developpement des aortes posterieures chez I'embryon de

poulet. C. R. Soc. Biol., T. III. Paris, 1891.

Developpement des aortes chez Tembryon de poulet. Journ. de

Tanat. et phys., T. XXVIII, 1892. ZucKERKANDL, E., Zur Anat. und Entwickelungsgeschichte der Arterien des

Unterschenkels und des Fusses. Anat. Hefte, Bd. V, 1895.

Zur Anatomie und Entwickelungsgeschichte der Arterien des Vor derarmes. Anat. Hefte, Bd. IV, 1894.

LITERATURE — CHAPTER XIII

Abraham, K., Beitrage zur Entwickelungsgeschichte des Wellensittichs.

Anat. Hefte, Bd. XVII, 1901. Balfour, F. M., On the Origin and History of the Urogenital Organs of

Vertebrates. Journ. of Anat. and Physiol., Vol. X, 1876. Balfour and Sedgwick, On the Existence of a Rudimentary Head Kidney

in the Embryo Chick. Proc. R. Soc, London, Vol. XXVII, 1878. On the Existence of a Head Kidney in the Embryo Chick and on

Certain Points in the Development of the Miillerian Duct. Quar. Journ.

Micr. Sc, Vol. XIX, 1879. BoRNHAUPT, Th., Zur Entwickelung des Urogenitalsystems beim Huhnchen.

Inaug. Diss. Dorpat, 1867. Brandt, A., Ueber den Zusammenhang der Glandula suprarenalis mit dem

parovarium resp. der Epididymis bei Hiihnern. Biolog. Centralbl.,

Bd. IX, 1889.

Anatomisches und allgemeines liber die sog. Hahnenfedrigkeit und

liber anderweitige Geschlechtsanomalien der Vogel. Zeitschr. wiss. Zool.,

Bd. XL VIII, 1889. Felix, W., Zur Entwickelungsgeschichte der Vorniere des Huhnchens Anat. Anz., Bd. V, 1890. Felix und Buhler, Die Entwickelung der Ham- und Geschlechtsorgane.

]. Abschnitt — Die Entwickelung des Harnapparates, von Prof. Felix.

Handbuch der vergl. u. exper. Entw.-lehre der Wirbeltiere, HIS 1904. FiRKET, Jean, Recherches sur I'organogenese des glands sexuelles chez les

oiseaux. Arch, de Biol. Tome 29, pp. 201-351. PI. 5, 1914. FuRBRiNGER, M., Zur vcrgleichendeu Anatomie und Entwickelungsgeschichte

der Excretionsorgane der Vertebraten. Morph. Jahrb., Bd. IV, 1878. Fusari, R., Contribution a I'etude du developpement des capsules surre nales et du sympathetique chez le poulet et chez les mamniiferes. Archives. Hal. de biologic, T. XVI, 1892.


460 APPEXDIX

Gasser, E., Beitrage zur Entwickelungsgeschichte der Allantois, der Muller schen Gange imd des Afters. Frankfurt a. M., 1874.

Die Entstehung des Wolff'schen Ganges beim Huhn. Sitz.-ber.

Naturf. Ges., Marburg, Jahrg. 1875.

Beobachtungen uber die Entstehung des Wolff'schen Ganges bei

Embryonen von Hiihnern und Gansen. Arch. mikr. Anat.. Bd. XIV, 1877. Gasser, E., und Siemmerling, Beitrage zur Entwickekmg des Urogenitalsys tems bei den Huhnerembryonen. Sitz.-ber. Naturf. Ges., Marburg, 1879. Gerhardt, U., Zur Entwickelung der bleibenden Niere. Arch. mikr. Anat.,

Bd. LVII, 1901. HocHSTETTER, F., Zur Morphologie der Vena cava inferior. Anat. Anz., Bd. Ill,

1888. Hoffmann, C. K., Etude sur le developpement de I'appareil urogenital des

oiseaux. Verhandelingen der Koninklyke Akademie van Wetenschap pen. Amsterdam, Tweede Sectie, Vol. I, 1892. Janosik, J., Bemerkungen iiber die Entwickelung der Nebennieren. Archiv.

mikr. Anat., Bd. XXII, 1883.

Histologisch-embryologische Untersuchungen iiber das Urogenital system. Sitzungsber. Akad. Wiss. Wien, math.-nat. Kl., Bd. XCI,

3. Abth., 1885. KosE, W., Ueber die Carotisdriise und das "Chromaffine Gewebe" der Vogel.

Anat. Anz., Bd. XXV, 1904. KowALEvsKY, R., Die Bildung der Urogenitalanlage bei Huhnerembryonen.

Stud. Lab. Warsaw Univ., II, 1875. KuPFFER, C, Untersuchungen iiber die Entwickelung des Harn- und Ge schlechtssystems. Arch. mikr. Anat., Bd. I, 1865; and ibid. Bd. II, 1866. V. MiHALCOVics, v., Untersuchungen iiber die Entwickelung des Harn und Geschlechtsapparates der Amnioten. Intern. Monatschr. Anat.

und Phys., Bd. II, 1885-1886. Miner viNi, R., Des capsules surrenales: Developpement, structure, fonc

tions. Journ. de Tanat. et de la phys, An. XL. Paris, 1904. NussBAUM, M., Zur Differenzierung des Geschlechtes im Thierreich. Arch.

mikr. Anat., Bd. XVIII, 1880.

Zur Entwickelung des Geschlechts beim Huhn. Verh. anat. Ges., Bd

XV, 1901.

Zur Riickbildung embryonaler Anlagen. Arch. mikr. Anat., Bd

LVII, 1901.

Zur Entwickelung des Urogenitalsystems beim Huhn. C. R. Ass.

d. An. Sess., 5. Liege, 1903. Poll, H., Die Entwickelung der Nebennierensysteme. Handbuch der

vergl. und exper. Entwickelungslehre der Wirbeltiere. III^ 1906. Prenant, a., Remarques a propos de la constitution de la glande genitale

indifferente et de I'histogenese du tube seminifere. C. R. Soc. biol.,

Ser. 9, T. II, 1890. Rabl, H., Die Entwickelung und Struktur der Nebennieren bei den Vogeln.

Arch. mikr. Anat., Bd. XXXVIII, 1891. Renson, G., Recherches sur le rein cephalique et le corps de Wolff chez les

oiseaux et les mammiferes. Arch. mikr. Anat., Bd. XXII, 1883.


APPENDIX 461

RucKERT, J., Entwickelung der Excretionsorgane. Ergebnisse der Anat.

u. Entw.-gesch., Bd. I, 1892. ScHREixER, K. E., Ueber die Entwickelung der Amniotenniere. Zeitschr.

wiss. Zool., Bd. LXXI, 1902. Sedgwick, A., Deve opment of the Kidney in its Relation to the Wolffian Body in the Chick. Quart. Journ. IMicr. Sc, Vol. XX, 1880.

On the Early Development of the Anterior Part of the Wolffian Duct and Body in the Chick, together with Some Remarks on the Excretory System of Vertebrata. Quart. Journ. Micr. Sc, Vol. XXI, 1881. Semon, Richard, Die indifferente Anlage der Keimdriisen beim Htihnchen und ihre Differenzierung zum Hoden. Jen. Zeitschr. Naturwiss., Bd. XXI, 1887. SouLiE, E. H., Recherches sur le developpement des capsules surrenales chez les vertebres superieurs. Journ. de I'anat. et phys., Paris, An. XXXIX, 1903. Swift, Charles H., Origin and Early History of the Primordial GermCells in the Chick. American Journal of Anat., Vol. 15, pp. 483516, 1914.

Origin of the Definitive Sex-Cells in the Female Chick and their Relation to the Primordial Germ-Cells. ib. Vol. 18, pp. 441-470, 1915.

Origin of the Sex-Cords and Definitive Spermatogonia in the Male Chick, ib. Vol.20, pp. 375-410, 1916. Waldeyer, W., Eierstock und Ei. Ein Beitrag zur Anatomie und Ent wickelungsgeschichte der Sexualorgane. Leipzig, 1870. Weldon, On the Suprarenal Bodies of Vertebrates. Quar. Journ. Micr. Sc, Vol. XXV, 1884.

LITERATURE — CHAPTER XIV

Agassiz, L., On the Structure of the Foot in the Embryo of Birds. Proc

Boston Soc Nat. Hist., 1848. Bizzozero, G., Neue Untersuchungen iiber den Bau des Knochenmarks der

Vogeln. Arch. mikr. Anat., Bd. XXXV, 1890. See also Arch. Ital. de

Biol., T. XIV, 1891. Blu.mstein-Judixa, Beila, Die Pneumatisation des Markes der Vogelkno chen. Anat. Hefte, Abth. I, Bd. XXIX, 1905. Bracket, A., Etude sur la resorption de cartilage et le developpement des

OS longs chez les oiseaux. Internat. Monatschr. Anat. und Phys., Bd.

X, 1893. Braun, M., Entwickelung des Wellenpapageis. Arb. Zool. Zoot. Inst. Wiirz burg, Bd. V, 1881. Brulle et HuGUENY, Developpement des os des oiseaux. Ann. Sc. Nat.,

Ser. Ill, Zool. T. IV,1845. BuNGE, A., Untersuchungen zur Entwickelungsgeschichte des Beckengiirtels

der Amphibien, Reptilien und Vogel. Inaug. Diss. Dorpat. 1880. CuviER, Extrait d'un memoire sur les progres de I'ossification dans le sternum

des oiseaux. Ann. des Sc Nat., Ser. I, Vol. XXV, 1832. V. Ebner, v., Ueber die Beziehungen der Wirbel zu den LTrwirbel. Sitzungsber.

d. k. Akad. d. Wiss. Wien, math.-naturwiss. Kl., Bd. CI, 3. Abth.. 1892.


462 APPENDIX

Urwirbel und Neugliederiing der Wirbelsaule. Sitzungsber. d. k.

Akad. d. Wiss. Wien, Bd. XCVII, 3. Abth. Wien, 1889, Jahrg., 1888. Froriep, a., Zur Entwickelungsgeschichte der Wirbelsaule, insbesondere

des Atlas und Epistropheus und der Occipitalregion. I. Beobachtungen

an Hiihnerembryonen. Arch. Anat. u. Entw., 1883. Gaupp, E., Die Entwickelung des Kopfskelettes. Handbuch der vergl. u.

exper. Entw.-lehre der Wirbeltiere, Bd. 3, 1905.

Die Entwickelung der Wirbelsaule. Zool. Centralbl., Jahrg. Ill, 1896. Die Metamerie des Schadels. Ergeb. der Anat. u. Entw., 1897. Gegenbaur, C, Untersuchungen zur vergl. Anat. der Wirbelsaule bei

Amphibien und Reptilien. Leipzig, 1864.

Beitrage zur Kenntniss des Beckens der Vogel. Eine vergleichende

anatomische Untersuchung. Jen. Zeitschr. Med. u. Naturw., Bd. VI, 1871. Die Metamerie des Kopfes und die Wirbeltheorie des Kopfskelettes,

im Lichte der neueren Untersuchungen betrachtet und gepriift. Morph.

Jahrb., Bd. XIII, 1888. GoETTE, A., Die Wirbelsaule und ihre Anhange. Arch. mikr. Anat., Bd.

XV, 1878. Hepburn, D., The Development of Diarthrodial Joints in Birds and Mammals. Proc. R. Soc. Edinb., Vol. XVI, 1889. Also in Journ. of Anat.

and Phys., 1889. Jager, G., Das Wirbelkorpergelenk der Vogel. Sitzungsber. Akad. Wien,

Bd. XXXIII, 1858. Johnson, Alice, On the Development of the Pelvic Girdle and Skeleton

of the Hind Limb in the Chick. Quar. Journ. Micr. Sc, Vol. XXIII,

1883. KuLCZYCKi, W., Zur Entwickelungsgeschichte des Schultergiirtels bei den

Vogeln mit besonderer Berucksichtigung des Schliisselbeines (Gallus,

Columba, Anas). Anat. Anz., Bd. XIX, 1901. Leighton, V. L., The Development of the Wing of Sterna Wilsonii. Am.

Nat., Vol. XXVIII, 1894. LuHDER, W., Zur Bildung des Brustbeins und Schultergiirtels der Vogel.

Journ. Ornith., 1871. Mannich, H., Beitrage zur Entwickelung der Wirbelsaule von Eudyptes

chrysocome. Inaug. Diss. Jena, 1902. Mehnert, Ernst, LTntersuchungen liber die Entwickelung des Os Pelvis

der Vogel. Morph. Jahrb., Bd. XIII, 1887.

Kainogenesis als Ausdruck differenter phylogenetischer Energieen.

Morph. Arb., Bd. VII, 1897. Morse, E. S., On the Identity of the Ascending Process of the Astragalus

in Birds w'ith the Intermedium. Anniversary Mem. Boston Soc. Nat.

Hist., 1880. Norsa, E., Alcune richerche sulla morphologia dei membri anteriori degli

uccelli. Richerche fatte nel Laborat Anatomico di Roma e alti labora tori biologici, Vol. IV, fasc. I. Abstract in French in Arch. Ital. biol.,

T. XXII, 1894. Parker, W. K., On the Structure and Development of the Skull of the Common Fowl (Gallus domesticus). Phil. Trans., Vol. CLIX, 1869.


APPEXDIX 463

Parker, W. K., On the Structure and Development of the Birds' Skull.

Trans. Linn. Soc, 1876.

On the Structure and Development of the Wing of the Common Fowl.

Phil. Trans., 1888. Remak, R., Untersuchungen liber die Entwickelung der Wirbeltiere. Berlin,

1850-1855. Rosenberg, A., Ueber die Entwickelung des Extremitiitenskelets bei einigen

durch die Reduction ihrer Gliedmaassen charakteristischen Wirbeltiere.

Zeitschr. wiss. ZooL, Bd. XXIII, 1873. ScHAUiNSLAND, H., Die Entwickelung der Wirbelsaule nebst Rippen und

Brustbein. Handbuch der vergl. und exper. Entw.-lehre der Wirbeltiere, Bd. Ill, T. 2, 1905. Schenk, F., Studien liber die Entwickelung des knochernen Unterkiefers

der Vogel. Sitzungsber. Akad. Wien, XXXIV Jahrg., 1897. Schultze, O., Ueber Eml^ryonale und bleibende Segmentirung. Verh.

Anat. Ges., Bd. X. Berlin, 1896. Stricht, O. van der, Recherches sur les cartilages articulaires des oiseaux.

Arch, de biol., T. X, 1890. SuscHKiN, P., Zur Anatomic und Entwickelungsgeschichte des Schadels der

Raub vogel. Anat. Anz., Bd. XI, 1896.

Zur Morphologic des Vogelskeletts. (1) Schadel von Tinnunculus.

Nouv. Mem. Soc. Imp. des X'atur. de Moscow, T. X\T, 1899. ScHWARCK, W., Beitrage zur Entwickelungsgeschichte der Wirbelsaule bei

den Vogeln. Anat. Studien (Herausgeg. v. Hasse), Bd. I, 1873. WiEDERSHEiM, R., Ucbcr die Entwickelung des Schulter- und Beckenglirtels.

Anat. Anz., Bd. IV, 1889, and V, 1890. WiJHE, J. W. VAN, Ueber Somiten und Nerven im Kopfe von Vogel- und

Reptilienembryonen. Zool. Anz., Jahrg. IX, 1886.


INDEX


Abducens nerve, 267

Abducens nucleus, 262, 263

Abnormal eggs, 2.5

Accessory cleavage of pigeon's egg, 38, 43, 44

Accessory mesenteries, 340, 341

Acustico-facial ganglion complex, 159 160, 262, 268

Air-sacs, 326, 330, 331

Albumen, 18

Albumen-sac, 217, 224

Albuginea of testis, 397

Alecithal ova (see isolecithal)

Allantois, blood-supply of, 222; general, 217; inner wall of, 220; neck of, 143, 144, 316; origin of, 143, 144; outer wall of, 220; rate of growth, 221; structure of inner wall, 223; structure of outer wall, 223

Amnion, effect of rotation of embryo on, 140, 141, 142; functions of, 231; head fold of, 137, 139; later history of, 231; mechanism of formation, 139, 140; muscle fibers of, 231; origin of, 135; secondary folds of, 142

Amnio-cardiac vesicles, 92, 116

AmpuUse of semicircular canals, 291

Anal plate, 143, 182

See also cloacal membrane

Angioblast, 88

Anterior chamber of eye, 278

Anterior commissure of spinal cord, origin of, 244

Anterior intestinal portal, 95 (Fig. 49), 121, 132

Anterior mesenteric artery, 363

Aortic arches, 198, 199, 203, 358362 ; transformations of, 359-361

Appendicular skeleton, 434

Aqueduct of Sylvius, 251.

Archenteron, 55

Area opaca, 39, 50, 61, 86; pellucida, 39, 50, 61; vasculosa, 61, 86; vitellina, 61, 62, 86

Arterial system, 121, 126, 198, 199, 203, 204, 228, 358-363

Atlas, development of, 420

Atrium bursse omentalis, 344


Auditory nerve, 295; ossicles, 299, 432; pit, 168

Auricular canal, 354

Auriculo- ventricular canal, 348; division of, 355

Axis, development of, 420

Axones, origin of, 235

Basilar plate, 429

Beak, 302, 304

Biogenesis, fundamental law of, 4

Blastoderm, 17; diameter of unin cubated, 61; expansion of, 50, 53,

61 Blastopore, 55, 82 Blood-cells, origin of, 118 Blood-islands, origin of, 86, 89 Blood-vessels, origin of, 118 Body-cavity, 115, 205-210, 333 Bony labyrinth, 296 Brain, primary divisions of, 108;

early development of, 147, 156;

later development of, 244-252 Branchial arch, first, skeleton of, 432 Bronchi, 325, 326 Bulbus arteriosus, 198, 201, 202, 348;

fate of, 357 Bursa Fabricii, 314, 317, 319 Bursa omenti ma j oris, 344 Bursa omenti minoris, 344

Canal of Schlemm, 279

Cardinal veins, anterior, 200, 204,

205, 363; posterior, 200, 204, 205,

368 Carina of sternum, 427 Carotid arch, 361 Carotid, common, 362; external 359,

361 ; internal, 359-361 Carpus, 436, 437 Cartilage, absorption of, 408; bones,

definition, 407; calcification of,

409 Caval fold, 344 Cavo-coeliac recess, 344 Cavum sub-pulmonale, 342 Cell-chain hypothesis, 255 Cell theory, \

Central and marginal cells, 41, 42 Central canal of spinal cord, 242


465


466


INDEX


Cerebellum, 155, 251

Cephalic mesoblastic somites, 108, 269, 428

Cerebral flexures, 149, 245

Cerebral ganjilia, 157-162, 262

Cerebral hemispheres, origin of, 151; (see telencephalon)

Cervical flexure, 133, 245

Chalazee, 18

Chemical composition of parts of hen's egg, 20, 21

Chiasma opticus, 154, 249

Choanal, 215, 285

Chondrification, 408

Chorion, 135, 217, 218, 220

Choroid coat of eye. 279; fissure, 166, 281 ; plexus, 248

Chromaffin tissue, 404

Chronology, 64

Cilary processes, 272, 274

Circulation of blood, 121, 122, 197200, 372-376

Circulation of blood, changes at hatching, 376; completion of double, 355

Classification of stages, 64-67

Clavicle, 434, 435

Cleavage of ovum (hen), 39-43

Cleavage of ovum (pigeon), 43-47

Cloaca, 314-319; (see hind-gut)

Cloacal membrane, 315, 318; (see also anal plate)

Coeliac artery, 363

Coelome (see body-cavity)

Coenogenetic aspects of development, 6

Collaterals, origin of, 238

Collecting tubules of mesonephros, 379, 380

CoUiculus palato-pharyngeus, 398

Commissura anterior, 252; inferior, 252 ; posterior, 252 ; trochlearis, 252

Concrescence, theory of, 82, 84

Cones of growth, 235

Conjunctival sac, 279

Coprodseum, 315, 318, 319

Coracoid, 434, 435

Cornea, 278

Corpus striatum, 247

Corpus vitreum, 275

Cortical cords of suprarenal capsules, 405

Cranial flexure, 133, 245; nerves, 261

Cristse acusticse, 295

Crop, 312

Crural veins^ 372

Cushion septum, 355

Cuticle of sheU, 17

Cutis plate, 185, 188


Delimitation of embryo from blastoderm, 91

Dendrites, origin of, 236

Determinants, 7

Diencephalon, early development of, 152; later development of, 249

Dorsal aorta, origin of, 121

Dorsal longitudinal fissure and septum of spinal cord, 243, 244

Dorsal mesentery, 172, 342

Duct of Botallus, 359, 361, 376

Ducts of Cuvier, 200, 204, 207, 361

Ductus arteriosus (see duct of Botalus) ; choledochus (common bileduct), 181, 321; cochlearis, 293; cystico-entericus, 321 ; endolymphaticus, 169, 289; hepato-cysticus, 321; hepato-entericus, 321; venosus (see meatus venosus)

Duodenum, 310, 311

Ear, later development of, 288

Ectamnion, 138

Ectoderm and entoderm, origin of, 52

Ectoderm of oral cavity, limits of, 301

Egg, formation of, 22, 24, 25

Egg-tooth, 302, 303

Embryonic circulation, on the fou.rth day, 372-374; on the sixth day, 374; on the eighth day, 374-376

Embryonic membranes, diagrams of, 219, 220; general, 216; origin of, 135; summary of later historj^, 145

Endocardium, origin of, 119

Endolymphatic duct (see ductus endolymphaticus)

Endolymphatic sac (see saccus endolymphaticus)

Entobronch;, 327, 328

Entoderm, origin of, 52

Ependyma, origin of, 239

Epididymis, 391, 398

Epiphysis, 153, 249

Epiphyses (of long bones), 409

Epistropheus, development of, 420

Epithalamus, 251

Epithelial ceUs of neural tube, 233, 234

Epithelial vestiges of visceral pouches 309

Epoophoion, 401

Equatorial ring of lens, 277-278

Excentricity of cleavage, 41, 47

Excretory system, origin of, 190

External auditory meatus, 297, 300

External form of the embryo, 211

Eye, early development of, 164; later development of, 271

Eyelids, 279-280


INDEX


467


Facial region, development of the,

214, 215, 216 Facialis nerve, 268 Facialis nucleus, 262, 263 Femur, 440 Fertilization, 35 Fibula, 440

First segmentation nucleus, 36 Fissura metotica, 429 Foetal development, 11 Fold of the omentum, 344, 345 Follicles of ovary, 22, 26, 27, 28, 30,

400 Follicular cells, origin of, 27, 400 Foramen, interventricular, 353, 354;

of Monro, 247; of Winslow, 343;

ovale, 355 Foramina, interauricular, 355 Fore-brain, origin of, 108 Fore-gut, 91, 9'3, 172 Formative stuffs, 15 Funiculi prajcervicales, 307

Gall-bladder, 321

Ganglia, cranial and spinal, 156; cranial, 157, 158, 159, 262; spinal, later development of, 254, 257

Ganglion, ciliare, 266; geniculatum, 268; jugulare, 268; olfactorium nervi trigemini, 264; nodosum, 161, 268 ; ~ petrosum, 161, 268; of Remak, 257

Gastric diverticula of body-cavity, 340

Gastrulation, 53, 84

Genetic restriction, law of, 8

Genital ducts, development of, 401

Germ-cells, general characters of, 9-12; comparison of, 12-14

Germ-wall, 47, 48, 69, 90, 128, 129

Germinal cells of neural tube, 233, 234

Germinal disc, 11, 12, 35, 37, 39

Germinal epithelium, 391, 392, 399

Germinal vesicle, 27, 28

Gizzard, 313, 314

Glomeruli of pronephros, 192

Glossopharyngeus, ganglion complex of, 161, 262, 268; nerve, 268; nucleus, 262, 263

Glottis, 332

Gray matter of spinal cord, development of, 240; origin of, 239

Haemal arch of vertebrae, 416, 417

Harderian gland, 280

Hatching, 232

Head, development of, 213

Head-fold, origin of, 91

Head process, 73, 80


Heart, changes of position of, 348, 349; development on second and third days, 200-203; divisions of cavities of, 350 ; ganglia and nerves of, 259; later development of, 348; origin of, 119

Hensen's knot, 73

Hepatic veins, 366

Hepatic portal circulation, 366, 375

Hermaphroditism of embryo, 391

Heterotaxia, 133

Hiatus communis recessum, 343

Hind-brain, origin of, 108

Hind-gut, 143, 172

Hind-limbs, origin of skeleton, 438

Hoffmann's nucleus, 240

Holoblastic ova, 11, 12

Humerus, 436

Hyoid arch, 175: skeleton of, 432

Hyomandibular cleft, 174, 297

Hypoglossus nerve, 269

Hypophysis, 154, 249

Hypothalamus, 251

Ilium, 438, 439

Incubation, normal temperature for, 65, 66

Indifferent stage of sexual organs, 391

Infundibulum (of brain), 154, 249

Infundibulum (of oviduct). See ostium tubae abdominale

Interganglionic commissures, 156

Intermediate cell-mass, 114, 190

Interventricular sulcus, 348, 353

Intervertebral fissure, 412

Intestine, general development of, 310. 311

Iris, 272 : muscles of, 273, 274

Ischiadic veins, 372

Ischium, 438, 439

Isolecithal ova, 11

Isthmus, of brain, 155; of oviduct, 22

Jacobson, organ of, 286 Jugular vein, 363

Kidney, capsule of, 390; permanent, 384-389; secreting tubules of, 390

Lagena, 293

Lamina terminalis, 105, 152, 247, 248

Larva, 11

Laryngotracheal groove, 178, 331,

332 Ijarynx, 332 Latebra, 1 9

Lateral plate of mesoblast, 115 Lateral tongue folds, 305 Lens, 166, 276-278


468


INDEX


Lenticular zone of optic cup, 271

Lesser peritoneal cavity, 344

Ligamentum pectinatuni iridis, 279

Limiting sulci, 130

Lingual glands, 30G

Lip-grooves, 304

Liver, histogenesis of, 323; later development of, 319-323; origin and early development of, 179, 180, 181 ; origin of lobes of, 322 ; primarv ventral ligament of, 335

Lungs,^ 178, 326

Macula utriculi, sacculi, etc., 295

Malpighian corpuscles (mesonephric) origin of, 195

Mammillae of shell, 17

Mandibular aortic arch, 121, 122, 203, 204

Mandibular arch, skeleton of, 431

Mandibular glands, 306

Mantle layer of spinal cord, origin of, 239

Margin of overgrowth, 52, 57

Marginal notch, 60, 84, 85

Marginal velum, 235

Marrow of bone, origin of, 410

Maturation of ovum, 32

Meatus venosus, 199, 364, 366, 368

Medullary cords of suprarenal capsules, 405, 406

Medullary neuroblasts of brain, 262

Medullary plate, 95; position of anterior end of, in neural tube, 102, 103

Megaspheres, 59

Membrana reuniens, 418

Membrane bones, definition of, 407

]\Iembranes of ovum, 10

Membranous labyrinth, 289

Meroblastic ova, 11

Mesencephalon, 108, 155, 251

Mesenchyme, definition of, 116

Mesenteric artery, 363

Mesenteric vein, 366, 367

Mesenteries, 333

Mesentery, dorsal, 172, 342; of the vena cava inferior, 341

Mesoblast, gastral, 110; of the head, origin of, 116, 117; history of between 1 and 12 somites, 109; lateral plate of, 110, 115; of opaque area, origin of, 86, 88; origin of, 74, 78; paraxial, 110; prostomial, 110; somatic layer of, 115; splanchnic layer of, 115

Mesobronchus, 326, 327

Mesocardia lateralia, 200, 207, 334, 337

Mesocardium, origin of, 120


Mesogastrium, 309, 342, 343 Mesonephric arteries, 363 Mesonephric mesentery, 341 Mesonephric tubules, formation of,

195 Mesonephric ureters, 380 Mesonephros, later history of, 378;

origin and early history of, 194 197; see ^^'olffian body Mesothalamus, 251 Mesothelium, definition of, 116 Metacarpus, 436, 437, 438 Metamorphosis, 11 Metanephros, 384-389 Metatarsals, 441 Metathalamus, 251 Metencephalon, 155, 251 Mid-brain (see Mesencephalon) Mid-gut, 172, 181, 310 Mouth, 301 Miillerian ducts, 391; degeneration

in male, 402, 403; origin of, 401,

402, 403 Muscles of iris, 274 Muscle plate, 185, 186 Myelencephalon, 155, 252 Myocardium, origin of, 119 Myotome, 188

Nares, 286

Nephrogenous tissue, 195, 378; of

metanephros, 384, 387 Nephrotome, 114, 190 Neural crest, 156 Neural folds, 97, 99 Neural groove, 97 Neural tube, 95, 105 Neurenteric canal, 73, 82 Neuroblasts, 233-239; classes of, in

spinal cord, 244 Neurocranium, 427, 428 Neuroglia cells, origin of, 239, 240 Neuromeres, 108, 148, 152, 155 Neurone theory, 236, 255, 256 Neuropore, 101, 105 Notochord, later development of,

411 ff; oriirin of, 80; in the region

of the skull, 428

Oblicjue septum, 331, 342 Oculo-motor nerve, 265; nucleus,

262, 263 Odontoid process, origin of, 420 (Esophagus, 179, 310, 312 Olfactory lobe; 247 Olfactory nerve, 263 Olfactory pits, 169, 285 Olfactory A'estibule, 285 Omentum, development of, 343 Omphalocephaly, 120


INDEX


469


Omphalomesenteric arteries, 199,363; veins, 364-366

Ootid, 14

Opaque area, see area opaca

Optic cup, 165, 271 ; lobes, 251 ; nerve, 2S3, 284, 285; stalk, 149, 164, 284, 285; vesicles, accessory, 164

Optic vesicles, primary, 108, 164; secondary, 166

Ora serrata, 272

Oral cavity, 215, 216, 301

Oral glands, 306

Oral plate, 95, 173

Orientation of embryo on yolk, 25, 63

Ossification, 408-411; endochondral, 409; perichondral, 408

Ostium tubse abdominale, 23 ; development of, 402, 403; relation to pronephros, 402

Otocyst, 168; later development of, 289; method of closure, 168

Ovary, 22, 398-401; degeneration of right, 398

Oviducal membranes of ovum, 10

Oviduct, 22; later development of, 403

Ovocyte, 13, 26, 27

Ovogenesis, 12, 26

Ovogonia, 12, 26

Ovum, 2. 10; bilateral symmetry of, 15; follicular membrane of, 10; organization of, 14; polarity of, 14

Palate, 285, 299

Palatine glands, 306

Palingenetic aspects of development,

6 Pancreas, 181, 323-325, 347 Pander's nucleus, 19 Papilla; conjunctivie sclerse, 280 Parabronchi, 328 Parachordals, 428, 429 Paradidvmis, 391, 398 Paraphysis, 248 Parencephalon, 108, 153, 249 Parietal cavity, 92, 116, 207, 208,

333, 334 Paroophoron, 401 Pars copularis (of tongue), 305 Pars inferior iabyrinthi, 289,. 293 Pars superior lal)yrinthi, 2S9, 291 Parthenogenetic cleavage, 35 Patella, 441 Pecten, 281, 282 Pectoral girdle, 434-436 Pellucid area (see area pellucida) Pelvic girdle, 438-440 Periaxial cords, 158, 159, 161 Pericardiaco-peritoneal membrane,

338


Pericardial and pleuroperitoneal cavities, separation of, 333

Pericardium, closure of dorsal opening of, 337; formation of membranous, 338; see parietal cavity.

Periblast, 38, 43, 47; marginal and central 48; nuclei, origin of, 47, 48

Perichondrium, 408

Periderm, 304

Perilymph, 296, 297

Periosteum, 409

Peripheral nervous system, development of, 252

Pfliiger, cords of, 399

Phseochrome tissue, 404

Phalanges, 436, 438; of foot, 441; of wing, 438

Pharynx, derivatives of, 306; early development of, 93-95, 173; postbranchial portion of, 178

Phvlogenetic reduction of skeleton, 411

Physiological zero of development, 65

Physiology of development, 6

Pineal bodv, 153, 249

Placodes, 160, 161

Pleural and peritoneal cavities, separation of, 340

Pleural grooves, 208, 209

Pleuro-pericardial membrane, 338

Pleuroperitoneal membrane, 326; septum, 340, 341

Plica encephali ventralis, 149, 245

Plica mesogastrica, 341, 344, 368

Pneumato-enteric recesses, 209, 340

Pneumatogastric nerve, 268

Polar bodies, 13, 34

Polyspermy, 35, 36, 37

Pons, 252

Pontine flexure, 149, 245

Postanal gut, 182

Postbranchial bodies, 307, 309

Posterior intestinal portal, 132

Postotic neural crest, 160, 161

Precardial plate, 334, 338

Preformation, 6

Pre-oral gut, 174

Pre-oral visceral furrows, 174, 175

Preotic neural crest, 158

Primitive groove, 72

Primitive intestine, 55

Primitive knot, 73

Primitive mouth, 55, 82

Primitive ova, 26, 392, 399

Primitive pit, 73

Primitive plate, 73

Primitive streak, 69; interpretation of, 82; origin of, 74; relation to embryo, 85

Primordia, embryonic, 8


470


INDEX


Primordial cranium, development of,

428 Primordial follicle, 27 Proamnion, 86, 138 Procoracoid, 435 Proctoda^um, 170, 314, 319 Pronephros, 190-193 Pronucleus male and female, 34, 36 Prosencephalon, 108, 149 Proventriculus, 313 Pubis, 438, 439 Pulmo-enteric recesses (see pneu mato-) Pulmonary arteries, 359 Pupil of eye, 166, 272

Radius, 436

Ramus communicans, 254, 257, 259

Recapitulation theory, 3; diagram of, 5

Recessus hepatico-entericus, 343 ; recessus mesenterico-eutericus, 343; recessus opticus, 153; recessus pleuro-peritoneales, 340; recessus pulmo-hepatici, 340; recessus superior sacci omenti, 340

Rectum, 317

Renal corpuscles, 378, 383

Renal portal circulation, 369, 372, 375

Renal veins, 372

Reproduction, development of organs of, 390-403 ^

Respiratory tract, 178, 325

Rete testis, 398

Retina, 274, 275

Retinal zone of optic cup, 271

Rhombencephalon, 108, 155

Ribs, development of, 424, 425

s (abbreviation for somites), 67

Sacrum, 424

Sacculus, 293, 294

Saccus endolymphaticus, 169, 289, 290

Saccus infundibuli, 249

Scapula, 434, 435

Sclerotic coat of eye, 279

Sclerotomes, and vertebral segmentation, 412; components of, 412; occipital, 428; origin of, 185, 186

Seessell's pocket, 174

Segmental arteries, 122, 199, 362

Segmentation cavity, 43, 47, 53 (see also subgerminal cavity)

Semeniferous tubules, 398

Semicircular canals, 291

Semi-lunar valves, 352

Sensory areas of auditory labyrinth, origin of, 296


Septa of heart, completion of, 355,

356, 357 Septal gland of nose, 287 Septum aortico-pulmonale, 351, 352; of auricular canal, 355 ; bulboauricular, 353; cushion, 351, 355; interauricular, 351, 354; interventricular, 351, 353, 354; of sinus venosus, 358

Septum transversum, 208, 209, 334; derivatives of, 339; lateral closing folds of, 334, 337 ; median mass of, 335

Septum trunci et bulbi arteriosi, 351

Sero-amniotic connection, 138, 143, 217

Sexual cords, 393, 394; of ovary, 398; of testis, 395

Sexual differentiation, 394, 395

Sheath cells, 255

Shell, structure of, 17

Shell membrane, 18

Sickle (of Roller), 71

Sinu-auricular aperture, 357, 358

Sinu-auricular valves, 358

Sinus terminalis 86 (see also vena terminalis)

Sinus venosub, 197, 200, 201, 357; horns of, 358; relation to septum transversum, 339

Skeleton, general statement concerning origin, 407

Skull, chondrification of, 429-432; development of, 427; ossification of, 432, 433, 434

Somatopleure, 62, 115

Somite, first, position in embryo. 111

Somites, of the head, 114; mesoblastic, origin of, 110, 111; mesoblastic, metameric value of, 184; primary structure of, 114

Spermatid, 13

Spermatocyte, 13

Spermatogenesis, 12

Spermatogonia, 13

Spermatozoa, period of life Avithin oviduct, 35

Spermatozoon, 9

Spina iliaca, 440

Spinal accessory nerve, 269

Spinal cord, development of, 239

Spinal nerves, components of, 254; development of, 252, 255; bomatic components of, 254; splanchnic components of, 256

Splanchnocranium, 427

Splanchnopleure, 62, 115

Spleen, 345-347

Spongy layer of shell, 17

Stapes, 300


INDEX


471


Sternum, development of, 425-427

Stigma of follicle, 25

Stomach, 179, 313

Stomodaeum, 170, 173

Stroma of gonads, 393 ; of testis, 397

Subcardinal veins, 368, 369

Subclavian artery, 362

Subclavian veins, 363, 364

Subgerminal cavity, 53, 61, 69

Subintestinal vein, 367

Subnotochordal bar, 416, 418

Sulcus lingualis, 298

Sulcus tubo-tympanicus, 298

Supraorbital sinus of olfactory cavity, 285

Suprarenal capsules, 403-406

Sutura cerebralis anterior, 103-105; neurochordalis seu ventralis, 105; terminalis anterior, 105

Sympathetic nervous system, 256261; relation to suprarenals, 406

Sympathetic trunks, primary, 257; secondary, 258

Synencephalon, 108, 153, 249

Syrinx, 332

Tables of development, 68

Tail-fold, 131

Tarsuh, 441

Tectum lobi optici, 251

Teeth, 304

Tela choroidea, 152

Telencephalon and diencephalon,

origin of, 150 Telencephalon, later development of,

245-249; medium, 151, 245 Telolecithal, 11 Ten somite embryo, description of,

122 Testis, 395-398 Tetrads, 33

Thalami optici, 154, 251 Thymus, 308 Thyroid, 178, 307 Tongue, 305 Torus transversus, 248 Trabeculee, of skull, 428, 429; of

ventricles, 353 Trachea, 331, 332 Trigeminal ganglion complex, 160,

267 Trigeminus nerve, 267 ; nucleus (motor), 262, 263 Trochlearis nerve, 266; nucleus, 262,

263 Truncus arteriosus, 198 Tubal fissure, 298, 301 Tubal ridge, 401

Tuberculum impar (of tongue), 305 Tuberculum posterius, 249


Tubo-tympanic cavity, 297-300

Tubules of mesonephros, degeneration of, 380-382; formation of, 195-196; primary, secondary, tertiary, 379, 380

Turbinals, 285, 286, 431

Turning of embryo, 133

Tympanum, 297, 300

Ulna, 436

Umbilical arteries, 363; veins, 367,

368 Umbilicus, 144; of yolk-sac, 216 UnincuVjated blastoderm, structure

of, 69 Ureter, origin of, 384 Urinogenital ridge, 390, 391; system,

later development of, 378, etc. Uroda}um, 314, 319 Uterus, 22 Utriculus, 291, 292 Uvea, 273

Vagina, 22

Vagus, ganglion complex of, 161; nerve, 268; nucleus, 262, 263

Variability, embryonic, 64

Vas deferens, 401

Vasa efferentia, 398

Vascular system, anatomy of, on fourth day, 197-200; origin of, 117

Venous system, 127, 199, 204, 205, 228, 363-372

Velum transversum, 150, 248

Vena cava, anterior, 363, 364; inferior, 368-372

Vena porta sinistra, 367

Vena terminalis, 228; see also sinus terminalis

Ventral aorta, 121

Ventral longitudinal fissure of spinal cord, 243

Ventral mesentery, 131, 182, 343

Vertebrae, articulations of, 421; coalescence of, 424; costal processes of, 418; hypocentrum of, 418; intervertebral ligaments of, 421; ossification of, 421-424; pleurocentrum of, 418; stage of chondrification of, 418; suspensory ligaments of, 421 ;

Vertebral column, 411; condition on fourth day, 414; condition on fifth day, 415, 417; condition on seventh and eighth days, 418, 420; membranous stage of, 414 Vertebral segmentation, origin of,

412 ff Visceral arches, 175; clefts, 174, 307; furrows, 174; pouches, 174;


472


INDEX


/


pouches, early development of, 175178; pouches, fate of, 307, 308

Vitelline membrane, 10, 30, 31

Vitreous humor, 275


ongm


White matter of spinal cord,

of, 239, 241 Wing, origin of skeleton of, 434, 436 Wolffian body (see mesonephros) ; atrophy, 380, 382, 401; sexual and non-sexual portions, 396; at ninetv-six hours, 379; on the sixth^day, 382; on the eighth day, 382, 383 ; on the eleventh day, 385


Wolffian duct, 191, 193, 194, 391, 401

Yolk, 17, 19; formation of, 29 Yolk-sac, 143, 225-231; entoderm

of, 50; blood-vessels of, 227-230;

septa of, 225-227; ultimate fate

of, 230, 231 Yolk-spheres, 19, 20 Yolk-stalk, 132, 225

Zona radiata, 10, 30, 31 Zone of junction, 52, 57 Zones of the blastoderm, 127-129

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