Book - Outlines of Chordate Development 5
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Kellicott WE. Outlines of Chordate Development (1913) Henry Holt and Co., New York.
|Outlines of Chordate Development 1913: 1. Amphioxus | 2. Early Frog | 3. Later Frog Organogeny | 4. Early Chick - Embryonic Membranes and Appendages | 5. Later Chick - Organogeny | 6. Early Mammal - Embryonic Membranes and Appendages | Figures|
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Chapter V The Later Development Of The Chick - Organogeny
IT remains now for us to describe the chief events. in the development of the systems and organs of the embryo, from the condition at which we left them, for the most part about the thirtieth hour. We shall limit this account to little more than the bare mention of the more important morphological alterations of structure, considering the systems separately.
The Nervous System
The Central Nervous System
We have already traced the development of the central nervous system up to the formation of the spinal cord and brain, and the establishment, in the latter, of the primary hind-, fore-, and mid-brains. In connection with the primary fore-brain we noted the rudiments of the optic vesicles, and in the primary hind-brain the series of six neuromeres, or brain segments, which are clearly distinguishable at the thirty-hour stage described.
Fig. 122. Neuromeres in the brain of the chick embryo. Dorsal views. From Von Kupffer (Hertwig's Handbuch, etc.) after Hill. A. Embryo of twenty-four hours; two pairs of somites. B. Embryo of twenty-four hours; five pairs of somites. C. Embryo of twenty-five and one-half hours; six pairs of somites. D. Embryo of twenty-six hours; seven pairs of somites, cp, Posterior limit of prosencephalon; fr, posterior limit of mesencephalon; ps, primitive streak; u, first somite; 1-11, neuromeres.
In earlier stages neuromeres have made a brief, transitory appearance in the fore- and mid-brains as well. Thus in the embryo of about twenty-three hours (4 pairs of somites), Hill has distinguished eleven neuromeres, all told. Of these three are in the region of the future fore-brain: these disappear about the twenty-sixth hour (7 pairs of somites). The midbrain includes only two neuromeres, which remain distinguishable until about the thirty-fifth hour (14 pairs of somites). The six neuromeres of the hind-brain are the best marked, and are visible for several days (Fig. 122).
The next important advance consists in the transverse constriction of the primary fore- and hind-brains each into two sections, making in all five regions in the brain. The primary fore-brain, or prosencephalon, is divided into the anterior telencephalon, or secondary fore-brain, and the posterior diencephalon, or bet ween- brain. Then following the undivided mid-brain, or mesencephalon, come the two divisions of the primary hind-brain, or rhombencephalon; the anterior of these is known as the metencephalon, the posterior as the myelencephalon. The myelencephalon continues directly into the spinal cord.
We may now proceed to describe the principal structures arising in connection with each of the secondary divisions of the brain.
The telencephalon includes only the first neuromere. This portion of the brain, it will be recalled, is directed backward beneath the fore-gut, its morphologically anterior end actually being directed postero-dorsally (Fig. 123). The telencephalon expands vertically and the optic vesicles remain connected with its ventral side. As the optic vesicles push out toward the surface of the head, their connections with the brain become narrowed as the optic stalks. The cavities of the vesicles remain continuous, through the stalks, with the cavity of the telencephalon (Fig. 127), and a median depression in the floor of the telencephalon, between the openings of the optic stalks, becomes well marked as the recessus options (Fig. 123). This optic recess, and a short stretch of the brain- wall immediately in front of it, not now distinct but differentiating later, together mark, morphologically, the true anterior end of the central nervous system.
Fig. 123. Sagittal sections through the head of the chick. In A the heart is shown in optical section. After Lillie. A. Of an embryo with twenty-two or -three pairs of somites (about forty-four hours) . B. Of an embryo with thirtynine pairs of somites (end of the fourth day), o, Auricle; am, amnion; ao, dorsal aorta; ba, bulbus arteriosus; cf, cranial flexure; D, diencephalon; dv, ductus venosus; e, epiphysis; h, hypophysis; i, infundibulum; ip, anterior intestinal portal; is, isthmus; I, rudiment of lung; li, liver; m, mandibular arch; Ms, mesencephalon; Mt, metencephalon; My, myelencephalon; n, notochord (degenerating) ; o, oral membrane (oral plate); oe, oesophagus; p.pharynx; P, parencephalon; r, optic recess; S, Seessel's pocket (preoral gut); st, stomach; sv, sinus venosus; Sy, synencephalon; T, telencephalon; th, rudiment of thyroid body; tp, tuber* culum posterius; v, ventricle; vt, velum transversum.
The anterior and lateral portions of the telencephalon now begin to expand, giving the effect of a constriction at its posterior limit. This apparent constriction of the dorsal wall of the fore-brain is the velum transversum, which marks the separation between telencephalon and diencephalon. In these early stages no other sharp distinction between these two regions can be determined.
Toward the close of the second day a pah- of lateral extensions of the telencephalon push out rapidly and expand dorsally, anteriorly, and posteriorly; these are the rudiments of the cerebral hemispheres. The cavity of the telencephalon is continued into the cerebral hemispheres as the lateral ventricles, known also as the first and second ventricles of the brain. The reduced median cavity of the telencephalon remains, forming the anterior portion of the third ventricle; the openings of the lateral ventricles out of the third ventricle are known as the foramina of Monro. The cerebral hemispheres enlarge rapidly and soon grow out, either side of the mid-line, far in front of, and above, the original extent of the telencephalon, which remains limited to a narrow median strip dorsally and anteriorly (Fig. 124). The ventral and lateral walls of the cerebral hemispheres soon become greatly thickened, as the corpora striata, or basal ganglia, which finally become so large that they nearly obstruct the lateral ventricles. Elsewhere the walls of the hemispheres remain comparatively thin.
Fig. 124. Median sagittal section through the brain of the chick of twelve to thirteen days. From Von Kupffer (Hertwig's Handbuch, etc.) ; c, Cerebellum; ca, anterior commissure; cd, notochord; ch, habenular commissure; ci, infundibular commissure; ck, central canal of spinal cord; cp, posterior commissure; cpa, anterior pallial commissure; cs, spinal commissure; cv, cavum cerebelli; cw, optic chiasma; dr, epiphysial gland; dt, decussation of the trochlear (IV) nerve; e, epiphysis; ei, paraphysis; hm, cerebral hemisphere; hy, hypophysis; J, infundibulum ; le, ependymal lamina of the roof of the fourth ventricle; lo, olfactory lobe; Ip, posterior lobe of cerebral hemisphere; M, mesencephalon; opt, optic chiasma; pch, choroid plexus third ventricle; pi, choroid plexus of fourth ventricle; re, epiphysial recess; ro, optic recess; s, saccus of infundibulum; si, posterior intracephalic furrow; tp, tuberculum posterius; <pi, tuberculum mammillare; tr, torus transversus; va, velum medullare anterius; vi, median ventricle of telencephalon; vp, velum medullare posterius.
The dorsal region of the original telencephalon remains embedded between the hemispheres. On its dorsal surface, immediately in front of the velum transversum, it becomes invaginated as the paraphysis. That part of its walls in front of the recessus opticus, as far as the level of the foramina of Monro, forms the lamina terminalis; this remains very thin except in its middle where the anterior commissure develops later.
The diencephalon includes the second and third neuromeres. Its antero-dorsal and antero- ventral limits are marked, respectively, by the velum transversum and the recessus opticus. Posteriorly it is marked off from the mesencephalon ventrally by an elevation in the floor, the tuberculum posterius, and dorsally by a broad depression of the wall (Fig. 123).
Like the telencephalon, this also is vertically extended. Its cavity forms, together with the median cavity of the telencephalon, the third ventricle. Just behind the recessus opticus the ventral and ventro-lateral walls are thickened as the optic chiasma, and just back of this is a well-marked evagination, the rudiment of the infundibulum. The lateral walls of the diencephalon remain thin for a time, but later become greatly thickened as the optic thalami. The roof remains thin and considerably expanded; in the region of the velum transversum the roof of the diencephalon and telencephalon becomes modified into the folded choroid plexus of the third ventricle (Fig. 124). *Back of this the diencephalic roof is evaginated as the tubular epiphysis or pineal body. Finally a thickening in the dorsal wall marks the posterior dorsal limit of the diencephalon; this is the rudiment of the posterior commissure.
The mesencephalon, or mid-brain, forms the topographically anterior part of the brain, projecting considerably in advance of all the other structures of the embyro (Figs. 113, 114, 123). It includes the fourth and fifth neuromeres. It remains relatively undifferentiated for a considerable period, but later its dorsal and dorso-lateral walls evaginate and thicken, forming the optic lobes, which include a part of the original cavity of the mesencephalon. The central portion of its cavity, now greatly restricted, remains as the aqueduct of Sylvius, or iter, continuing posteriorly from the third ventricle. The ventral and ventro-lateral walls of the mesencephalon thicken to form the great nervous pathways from the optic lobes to other centers, known as the crura cerebri. Back of the optic lobes the mesencephalon remains undilated as the isthmus, leading directly to the metencephalon (Fig. 124).
The metencephalon, lying dorsal to the anterior tip of the notochord, consists of only the sixth neuromere, and is thus very short. The cavity of the metencephalon is not separable from that of the succeeding section, the myelencephalon; together they are known as the fourth ventricle. The walls of the metencephalon thicken slowly, though steadily, during the early days of incubation. Later the dorsal and dorso-lateral regions become very greatly thickened, forming the cerebellar hemispheres, or cerebellum. The ventral and ventro-lateral walls also thicken very considerably to form the pons Varolii.
The myelencephalon, the last division of the brain, includes the seventh to eleventh neuromeres, indications of which remain visible, ventrally, until about the fourth day. Its cavity, as said above, is the fourth ventricle. The roof of this section remains thin and non-nervous, and ultimately forms the choroid plexus of the fourth ventricle. The ventral and ventrolateral walls become greatly thickened as the medulla oblongata or spinal bulb. This region becomes flexed ventrally forming the pontine flexure (Fig. 124). The cervical flexure, previously, mentioned, is gradually disappearing, but the original cranial flexure of the mesencephalic region remains as a permanent feature of the brain.
Posteriorly the elongated myelencephalon passes into the spinal cord. This is of lesser diameter than the medulla, and at first is vertically elongated with somewhat thickened lateral walls. Its cavity, the central canal, continuous with the fourth ventricle, is narrow but deep. The lateral walls continue to thicken and finally the cord becomes approximately circular in section, and its cavity is reduced to a very small tube by the fusion of its dorsal walls. The median dorsal and ventral walls of the cord remain thin. As the lateral walls begin to thicken their constituent cells become highly differentiated. The original epithelial elements of the neural tube become differentiated as the ependymal cells; these are non-nervous, supporting cells. The free ends of the ependymal cells, bordering the central canal, become ciliated. The embryonic nerve cells, or germinal cells, originally scattered through the epithelial cells, multiply rapidly and form both neuroblasls, which give rise to the gray matter of the cord, and non-nervous supporting cells or glia cells. From the neuroblasts various processes grow out, for the most part remaining within the central nervous system and forming in part the white matter. Some of the neuroblasts of the ventro-lateral regions (ventral cornua) send out processes which leave the central system as the components of the ventral or motor (efferent) roots of the spinal nerves.
From the functional standpoint the most important facts concerning the development of the central nervous system are the histogenetic processes going on in the different regions of the walls of the brain and cord, especially the establishment of the various centers (nuclei) and tracts. Although of the greatest importance and interest, all such details lie without the scope of this work. (Further information on this general subject is found, together with references to the literature, in Johnston's " Nervous System of the Vertebrates/' Philadelphia, 1906.)
The Cranial and Spinal Ganglia
These structures are derived from the neural crests, whose formation has already been described. The neural crests finally extend the entire length of the nervous system. In the trunk region they begin to extend laterally between the ectoderm and the mesodermal somites. In the intervals between successive somites the neural crest becomes interrupted, the cells apparently, though not certainly, being converted into mesenchyme. By this process each crest is broken into a metameric series of cell-groups. These groups are the rudiments of the spinal ganglia, and therefore also of the dorsal (afferent) roots of the spinal nerves. Each group contains neuroblasts as well as indifferent cells, and very early comes into close relation with the cells of the adjoining somite.
In the region of the somites of the head the neural crests are poorly developed, in correlation with the absence of ganglia in these segments. But throughout the remainder of the head they are well developed and form the rudiments of the ganglia and certain of the branches of the cranial nerves. As in the trunk region, the continuous crests are broken up by the conversion of certain regions into mesenchyme. The regions remaining form the rudiments of the ganglia of the X, IX, VIII, VII, and V cranial nerves. The ganglia of the IX and X nerves arise together and are divided, toward the close of the second day into separate cell-groups by the formation of the gill-pouches of the region (Fig. 130). Thus the ganglion of the IX nerve, ganglion petrosum, is left just above the third visceral arch, and that of the X nerve, ganglion jiigulare-nodosum, above the fourth and fifth visceral arches. Each of these acquires a connection with an ectodermal branchial sense organ, or placode, just above the second and third visceral pouches. These placodes are vestigial organs in terrestrial vertebrates, and this connection, as well as the existence of the placodes themselves, is of very brief duration.
The ganglia of the VII and VIII nerves arise in common, from an enlarged part of the crest lying immediately in front of the rudiment of the ear. This cell-group, the acusticofacialis ganglion (Fig. 114), connects with the brain in the region of the third neuromere of the myelencephalon. It also connects (about the forty-eighth hour) with a well-marked placode on the first visceral pouch. The ganglion of the V nerve, trigeminal ganglion, is the most anterior of the series (Fig. 130). It connects with the first neuromere of the myelencephalon and sends outgrowths into the regions of both upper and lower jaws, as the rudiments of certain branches of the V nerve. A part of the mesenchyme of the mandibular and hyoid arches is also formed from the cells of these rudiments, and especially from the neural crest anterior to the V ganglion. During an early stage in their formation from the crests, the rudiments of the V and VII ganglia connect with the surface ectoderm around the first visceral pouch, and appear to receive cells proliferated from this layer. This connection is not to be confused with the much later connections established by the VII, IX, and X ganglia with the epibranchial placodes.
Fig. 125. Transverse section, passing through the eyes and heart, of an embryo with about thirty-five pairs of somites (about seventy-two hours). From Lillie (Development of the Chick). Am., Amnion; Ao. t dorsal aorta; Atr., auricle; B.A., bulbus arteriosus; Ch.Fis., choroid fissure; Chor., chorion; D.C., ductus Cuvieri; Dienc., diencephalon; Lg., rudiment of lung;P.C., pericardial cavity; p.Ch., posterior chamber; pl.gr., pleural groove; V.c., posterior cardinal vein; Y.S., yolk-sac.
The Peripheral Nervous System
We must distinguish here between the spinal and cranial nerves. The spinal nerves, of which there are some thirtyeight pairs distinguishable at certain stages, all develop essentially alike, while the twelve pairs of cranial nerves may differ widely form one another and from the spinal nerves, in their development, as they do in morphology and in function.
A. THE SPINAL NERVES AND THE SYMPATHETIC SYSTEM
Each spinal nerve is a complex, including parts of unlike function and relation to other structures. For our present purposes it will be necessary to distinguish only the dorsal or afferent and the ventral or efferent portions, and in each of these the somatic (somatopleural) and splanchnic (splanchnopleural) pathways. Brief reference to the sympathetic system may be included here because it is obviously derived, to a certain extent, from the same rudiments as are the spinal nerves.
The rudiments of the somatic afferent portions of the spinal nerves are the cell-groups derived from the neural crests described above, i.e., the spinal ganglia. During the third day the neuroblasts of the spinal ganglia send out processes (axons, axis cylinder processes) in two directions, centripetally into the spinal cord, and centrifugally, meeting and joining the ventral root; the cell bodies thus remain as the spinal ganglion cells. The ventral root of each spinal nerve is efferent and is composed of outgrowths (axons) from both somatic and splanchnic neuroblasts located in certain regions of the ventral cornua of the spinal cord. The dorsal and ventral (afferent and efferent) roots unite a short distance from the cord forming the spinal nerve trunk. This trunk then immediately divides into three main branches (Fig. 126); first is given off ventrally a large branch to the sympathetic system, the ramus communicans (see below). These fibers are finally distributed to splanchnopleural derivatives, and are derived from both dorsal and ventral roots. The trunk then separates into dorsal and ventral branches, each containing fibers from both roots, which are distributed chiefly, though not wholly, to somatopleural structures, the integument and striated muscles. Opposite the limbbuds the spinal nerves accompany extensions of the somites into the limbs and provide their innervation, supplying the muscles and integument.
Meanwhile the sympathetic system has been forming. During the third day some of the neuroblasts of the spinal ganglia send out processes which extend downward toward the aorta; thus establish a pair of longitudinal cords, the primary sympathetic cords (Fig. 126). Other migratory neuroblasts from the spinal ganglia then form somewhat similarly, a pair of secondary sympathetic cords just above the primary cords. The secondary cords then become connected segmentally with the spinal ganglia, by processes from the secondary cord cells which extend back into the ganglia and through the dorsal spinal root into the spinal cord. The primary sympathetic cords give rise to the prevertebral plexuses, but otherwise disappear entirely during the sixth and seventh days. The secondary sympathetic cords are the rudiments of the major portion of the definitive sympathetic cords of the adult, and the groups of fibers connecting these cords with the spinal ganglia become the rami communicantes. The secondary sympathetic cords become ganglionated, and additional processes grow out, connecting with the ganglia derived from the primary cords, whose cell processes are finally distributed in a complex manner to the visceral surfaces. The cardiac plexus, and the plexuses of the viscera, arise chiefly from neuroblasts migrating along the X nerves from the hind-brain and X ganglion.
Fig. 126. Diagram of the chief elements of the sympathetic nervous then along the path thus marked out some of the neuroblasts of aorta; ap, aortic plexus; d, dorsal the spinal ganglia, and others (afferent) root of spinal nerve; g, spinal ganglion; t, intestine; m, from the Spinal Cord itself, mimesentery ; n, notochordjfl, Remak's gra t e to a position ventral to the ganglion; s, splanchnic plexus; sg, , r
sympathetic elements in intestinal Spinal COTO, around the dorsal wall; t, mesonephric tubules; v, o nr fo Thp^P Tniorfltnrv pplk ventral (efferent) root of spinal * Ca - ni g ra //, secondary sympathetic cord. i -i nerve; I, primary sympathetic cord;
Two other important groups of fibers pass by way of the rami communicantes; these are (1) the visceral afferent fibers belonging with the dorsal spinal root and ganglion, which pass by way of the sympathetic trunks to their distribution in the visceral sensory surfaces, and (2) the visceral efferent (motor) fibers from the spinal cord and ventral root, to their distribution in the visceral musculature. These latter fibers, although arising in the cord and forming an important part of the spinal nerve, are really to be regarded as components of the sympathetic system.
B. THE CRANIAL NERVES
The cranial nerves exhibit in their development a variety that parallels their diversity in morphology and in function. It is possible, however, to relate many of them to parts of the typical spinal nerves, and like these they have two sources, ganglia from the neural crests, and neuroblasts within the spinal cord. The details of their development are complicated and we may include here only a few of the more important facts in connection with each nerve. The more posterior cranial nerves show greater similarity to the spinal nerves, and as we pass forward they diverge more and more widely from this type.
The XII Cranial Nerve (Hypoglossus) . This is the nerve associated with that part of the cord which has most recently become included within the medulla, i.e., the region of the first four mesodermal segments. It arises as two pairs of roots, similar to the ventral spinal nerve roots, in the region of the last two segments of the head. The two roots join and the nerve then passes around, posteriorly to the last gill-pouch, to the floor of the pharynx, where it is distributed to the muscles of the tongue; it is thus visceral efferent.
The XI Cranial Nerve (Spinal Accessory). The development of this nerve in the chick is unknown. The XI nerve is to be regarded as a separated caudal portion of the X nerve and since it is visceral efferent (although supplying voluntary muscles in the higher vertebrates), its development is probably not unlike that of the visceral efferent elements of the X nerve.
The X Cranial Nerve (Vagus or Pneumogastric) . This large nerve is really a complex, consisting of the nerves associated with the third and fourth visceral pouches. It is chiefly visceral, both afferent and efferent, and in addition to its visceral-pouch branches, it sends branches back to certain of the viscera.
The formation of the primary vagus ganglion has been described. This divides into two parts, one remaining in its original position (ganglion nodosum), the other moving down between the fourth and fifth visceral arches (ganglion jugulare). Its ventral root is multiple, a large number of outgrowths from the cells of the medulla converging to the ganglion nodosum, from which connections are made with the sympathetic system. From the ganglion jugulare branches grow out to the gill- pouch region, and a large branch passes posteriorly to supply the thoracic and abdominal organs. Neuroblasts accompany these branches and later form the sympathetic ganglia of the organs innervated.
The IX Cranial Nerve (Glossopharyngeal) . This is to be regarded as a separate anterior portion of the vagus group. It is the nerve of the second visceral pouch (first branchial pouch) . Its development is essentially similar to that of the branchial portions of the X nerve, with which it forms a connection.
The VIII Cranial Nerve (Auditory). As already noted the VIII nerve arises in common with the VII. A posterior part of the common acustico-facialis ganglion becomes intimately related with the rudiment of the ear (auditory sac) and later differentiates in situ. It has no efferent fibers equivalent to the ventral spinal roots or to the efferent components of the cranial nerves so far described.
The VII Cranial Nerve (Facial). That portion of the acustico-facialis ganglion remaining after the differentiation of the VIII ganglion and nerve, remains as the geniculate ganglion of the VII nerve. This connects with the medulla in the usual fashion, and distally fibers grow out into the vicinity of the first or hyomandibular visceral pouch (spiracle) with which this nerve is primarily related. In the chick it is chiefly visceral efferent, but the development of these motor components is not known, although the cells composing its nuclei of origin in the medulla, have the usual position relative to other centers.
The V Cranial Nerve (Trigeminal) . The trigeminal ganglion derived from the neural crest connects with the medulla in the usual way and early becomes partially divided. From the smaller anterior portion (profundus ganglion) fibers grow forward as the deep ophthalmic branch, while from the posterior part (trigeminal ganglion proper) arise the branches distributed to the upper and lower jaws. This nerve is chiefly somatic afferent, its small efferent component developing typically, during the fourth day.
The IV and VI Cranial Nerves (Trochlear and Abducent). These two nerves have many characteristics in common. They are purely motor, distributed to muscles of the eye-ball (superior oblique and external rectus, respectively), and consequently have no ganglia outside the medulla. They appear relatively late (fourth day), the IV from the dorsal surface of the isthmus, the VI from the ventral side of the myelencephalon.
The III Cranial Nerve (Oculomotor). This too is chiefly motor, supplying the remaining muscles of the eye-ball. Its fibers grow out from the ventral side of the mid- brain and extend into the mesenchyme around the developing eye. Associated with its motor elements are afferent components growing out from the ciliary ganglion. The neuroblasts. forming the ciliary ganglion appear to migrate from the neural tube and from the profundus ganglion of the V nerve. These afferent fibers seem to arise in the muscles of the eye-ball.
The so-called / (Olfactory) and II (Optic) cranial nerves will be considered in connection with the development of the sense organs with which they are associated.
The Special Sense Organs
We have described in the preceding chapter the formation of the optic vesicles from the primary fore-brain, and the differentiation of the optic stalks, which remain related with the ventral side of the diencephalon either side of and posterior to the recessus opticus (Fig. 125). The optic stalks and vesicles are the rudiments of only the essential, or sensory (recipient) and nervous elements, of the eye. All of the other accessory parts of this complex organ are differentiated from other tissues.
While the tubular optic stalk remains comparatively short, the optic vesicle enlarges rapidly and soon (thirty hours) reaches the surface ectoderm of the head. The continued dilation of the vesicle occurs mostly above the level of the stalk, -which therefore remains related with the ventral side of the vesicle, as of the brain (Fig. 128). Now there appears a thickening of the ectoderm opposite the optic vesicle; this is the rudiment of the lens. Both the optic vesicle and the rudiment of the lens then proceed to invaginate, independently, but in the same direction (Figs. 127, 128).
The invagination of the optic vesicle, which converts it into the two-layered optic cup, is not a simple hemispherical invagination. The irivaginating region begins about in the middle of the outer wall of the vesicle and extends thence downward, to the attachment of the optic stalk, as a vertical groove. The distal wall of the vesicle rapidly folds in toward the proximal wall and nearly obliterates the original cavity of the vesicle, just as the invaginating endoderm of the Amphioxus gastrula obliterates the blastocoel. The result is the formation of a twolayered optic cup; its inner layer, which may now be distinguished as the retinal layer is already quite thickened, while its outer layer has become quite thin (Figs. 127, 128). The new cavity of the optic cup is the rudiment of the large posterior chamber of the eye. The cavity of the cup is at first widely open toward the lens and ectoderm, but its margin rapidly draws together somewhat. In the middle of the cup, opposite the lens, it remains open as the circular rudiment of the pupil. Ventrally from this the rim draws together more closely, leaving only a narrow slit-like opening extending from the pupil to the attachment of the optic stalk; this is known as the choroid fissure (Fig. 128). The choroid fissure remains open for several days and takes an important part in determining the course of the later development of the eye.
Fig. 127. Diagrams illustrating the development of the eye in the chick. After Froriep (slightly modified). A. Transverse section through part of the fore-brain and optic vesicles of a chick, late the second day of incubation. On the left the section passes through the optic stalk, on the right to one side of it. B. Transverse section through the optic vesicle and associated structures at the end of the second day. C. Same, slightly later. D. Section through the pupillary region of the eye, the latter part of the fifth day. a, Anterior chamber of eye; ec, ectoderm of head (epidermis); eck, ectoderm of cornea; F, cavity (or wall, in B) of fore-brain; i, inner or retinal layer of optic cup; ir, mesodermal rudiment of iris; I, lens; m, mesoderm; mk, mesoderm of cornea; o, outer or pigment layer of optic cup; t, optic stalk; v, cavity of primary optic vesicle (in C and D nearly obliterated by the invagination of the optic vesicle to form the optic cup).
We must now return to trace the formation of the lens. The ectodermal thickening mentioned above rapidly extends, and proceeds to invaginate toward the invaginating retinal layer. Its wall thickens as it invaginates simply, and soon after the invagination of the retinal layer is completed, the lens separates from the ectoderm, forming a flattened vesicle lying in the cavity of the optic cup.
Fig. 128. Diagrams of sections through the eye of the chick embryo at the end of the second day. After Lillie. The dorsal margin is toward the top of the page in A and B. A. Eye as viewed directly. B. Vertical section through the line x-cf, in A. C. Horizontal section through the line y-y, in A. cf. Choroid fissure; cv, cavity of primary optic vesicle; ec, superficial ectoderm of head; i, inner or retinal layer of optic cup; I, lens; o, outer or pigmented layer of optic cup; ol, opening of lens sac from surface of head; pc, posterior chamber of eye; s, optic stalk, continuous with the floor and lateral wall of the diencephalon.
These events are completed during the third day, and now the optic cup enlarges very rapidly for a time, forming a large cavity (posterior chamber) still open through the pupil and the choroid fissure. From the rudiments now established and from the surrounding mesenchyme, the parts of the fully formed eye are all derived. We may mention only a few of the more important events in the further history of the structures.
The optic cup extends ventrally as well as in other directions, so that the attachment of the optic stalk appears no longer connected with the ventral side, but rather with the middle of the proximal hemisphere, nearly opposite the pupil and lens; this is known as the fundus region. Associated with this change is a decided alteration in the character and relations of the choroid fissure, which will be described below.
About the sixth or seventh day the thick inner layer of the optic cup becomes clearly differentiated into a proximal or retinal zone, and a distal or lenticular zone. The former includes rather more than the proximal hemisphere, while the latter forms a broad band bordering the pupil. The retinal portion becomes transformed later into the sensory and nervous parts of the eye; the thin outer layer in the retinal zone of the cup is not sensory, but is transformed into the pigmented layer of the retina. Both the inner and outer layers of the cup in the lenticular zone share in forming the rudiments of the iris and ciliary process. The separation between the retinal and lenticular zones is marked in the developed eye by the ora serrata.
In the lenticular zone the thin outer layer fuses with the inner layer, becomes pigmented, and together with mesenchyme cells of the region they form the iris (Fig. 127, D). The proper muscles of the iris are not derived from the mesenchyme, but from bud-like outgrowths of the lenticular zone (ectoderm). The ciliary process is at first a series of folds of the lenticular zone around the base of the iris, but soon these folds are invaded by mesenchyme cells which form the muscles of the ciliary process.
During the expansion of the optic cup the margins of the choroid fissure have come into close apposition, nearly closing the fissure. Owing to the originally ventral attachment of the optic stalk the retinal layer is continuous, either side of the fissure, with the lower side of the stalk, and the connection extends through about one quadrant of the optic cup, i.e., from the fundus nearly around to the margin of the retinal zone. Some of the retinal layer cells form neuroblasts, and from these nerve processes (axons) grow out. along the inner surface of the retina toward the attachment of the optic stalk. Finally they extend, by way of the margin of the choroid fissure, into the stalk, from all parts of the retina, and thence into the wall of the diencephalon (optic thalami) to the' optic lobes. The consequent thickening of the ventral walls of the optic stalks forming the optic tracts, leads to the disappearance of the original cavity of the stalk. The solid stalks or optic tracts, are commonly known as the // cranial or optic nerves (Fig. 128).
In the meantime the free inner margins of the choroid fissure have extended up into the cavity of the optic cup (posterior chamber), and finally they fuse forming a low ridge, the whole length of the original fissure, enclosing between them a bit of mesenchyme which had extended into the fissure from without. Finally the lips of the fissure fuse together externally also, and the internal ridge is recognized as the rudiment of the pecten of the eye. This enlarges rapidly and ultimately forms a folded, fan-like organ, projecting some distance upward into the posterior chamber.
The general content of the posterior chamber, known as the vitreous humor, is formed from the innermost cells of the retinal and lenticular zones. These cells send out branching processes through the chamber and later add a secretion, the two materials together making up the humor.
Just after the rudiment of the lens separates from the surface ectoderm, its inner wall becomes thickened by the elongation of its single layer of cells. Finally then* elongation becomes so marked that the original cavity of the lens vesicle is obliterated and the lens become solid. The epithelium on its outer face remains simple. This primary lens vesicle forms only the nucleus of the final structure, for around this are laid down, beginning about the eighth day, a large number of concentric layers of cells, derived from the periphery of the lens region, where the thin outer lens epithelium becomes continuous with the thick inner layer. These cells are formed irregularly, but finally they assume a definite and regular arrangement. Layers are formed during the entire growth period of the organism and the number finally laid down is very large. At first the lens is in contact with the surface ectoderm, but it soon moves within the pupil, leaving a space between itself and the ectoderm. This is the beginning of the anterior chamber of the eye (Fig. 127, D); it extends beyond the margin of the iris, and soon becomes invaded by mesenchyme cells, part of which are added to the iris ; while others form the larger part of the cornea.
The cornea is only to a slight degree formed by the surface ectoderm without the iris and pupil; only its superficial epithelium is thus derived. The major portion of the cornea is derived from mesenchyme cells which first form a single layer within the ectodermal epithelium (Fig. 127, D), and then later enter in large numbers between these two epithelia, forming layers of corneal cells. From the mesenchyme surrounding the entire optic cup are derived the choroid and sclerotic coats of the eye-ball.
Like the eye, the fully formed ear is a complex, formed of elements of diverse origin, which become morphologically and functionally associated during development. The ear develops somewhat later than the eye, in the region of the myelencephalon. Making the customary distinction between the primary or sensory, and the secondary or accessory portions, we see that the true sensory portion is formed from the surface of the head, rather than the wall of the nervous system. The accessory parts are derived from the hyomandibular visceral pouch and the mesenchyme of the region.
The first indication of the ear appears about the thirtieth hour as a circular thickening in the ectoderm on the side of the head, just in front of the level of the first mesodermal somite. This patch enlarges, becomes depressed and invaginated, and about the beginning of the third day it has formed a considerable sac, the auditory sac or otocyst, connected with the surface by a narrow canal. The otocyst very early becomes vertically elongated and soon shows internally an oblique ridge on its inner or medial surface, indicating its division into an upper and inner part, and a lower and outer part, known respectively as the superior and inferior chambers. The superior chamber is extended vertically as a short tube with which the canal leading to the surface is connected. This tube is the rudiment of the endolymphatic duct (Fig. 129, A). On account of the dorsal expansion of the superior chamber along the outer side of the endolymphatic duct, the latter appears to open into the inner side rather than into the apex of the superior chamber. The narrow canal of the duct becomes closed during the fifth day, and the otocyst soon thereafter loses all connection with the surface ectoderm.
Fig. 129. Two stages in the development of the auditory organ of the chick. A. Hemiseoted model of the auditory sac (otocyst) just before its separation from the superficial ectoderm of the head. After Krause. B. Median view of a model of the left membranous labyrinth of an embryo of seven days and seventeen hours. After Rothig and Brugsch. a. Anterior vertical semicircular canal; aa, ampulla of anterior vertical semicircular canal; ap, ampulla of posterior vertical semicircular canal; d, ductus endolymphaticus; e, superficial ectoderm of head; I, lagena (cochlea); p, rudiment of posterior vertical semicircular canal; s, rudiment of saccule; u, utricle; x, connection between auditory sac and superficial ectoderm.
We may now mention the more important steps in the development of each of these three primary regions of the otocyst. The endolymphatic duct grows dorsally during the seventh and eighth days, and its extremity dilates forming the endolymphatic sac. This finally extends above the central nervous system, and lies embedded in the mesenchyme along the dorso-lateral surface of the myelencephalon.
The superior chamber of the otocyst gives rise to the semicircular canals and the utricle. The semicircular canals are indicated the fifth day, as three slight grooves in the wall of the superior chamber, approximately in the relative positions of the fully developed canals, save that the posterior canal is at first oblique to the other two. These grooves deepen and their margins meet converting them into canals, which remain open into the chamber at their extremities. The canals push out from the surface of the otocyst carrying a thin sheet of its wall which becomes perforated between the body of the superior chamber and the canals, leaving them free, except at their attached ends. The cavity of the superior chamber remaining, after the formation of the semicircular canals, is the utricle; this receives also the opening of the endolymphatic duct, and ventrally it opens into the inferior chamber of the otocyst. The ampullce of the canals appear as dilations very early (seventh day).
The inferior chamber of the otocyst is the seat of origin of the saccule and the lagena or cochlea. The saccule appears (seventh day) as a swelling on the inner or medial wall of the extreme upper (dorsal) end of the inferior chamber. The ventral end of this chamber pushes downward as the rudiment of the lagena or cochlea, while the intermediate region remains as the cochlear duct. The lagena grows out for some distance, turning inward (medially) at its tip, forming as a whole a hook-shaped structure (Fig. 129, B).
The epithelial lining of the otocyst has meanwhile become thinner, except in certain patches which mark the location of the maculce, cristce, and papillce of the fully formed ear. In these regions the epithelium assumes the typical characteristics of the acustic epithelium, and into each patch there extend nerve fibers (axons) from the cells of the VIII nerve ganglion, which is intimately fused with the antero-ventral face of the otocyst.
The mesenchyme surrounding the otocyst differentiates into various structures during the development of the otocyst. First is formed a membranous layer which fuses with the external surface of the complex otocyst and its derivatives, forming the membranous labyrinth. Surrounding this the mesenchyme forms a loose tissue which becomes the perilymph, and around all of this comes finally a dense mesenchyme where the cartilaginous and later the bony labyrinths are laid down.
We have thus far described only the structures of the internal ear. It remains now to mention the chief facts regarding the development of the middle and outer ears. These develop partly from the pharyngeal cavity, and partly from the region of the hyomandibular visceral pouch and the surrounding mesenchyme. The hyomandibular pouch develops in two parts, a large ventral portion corresponding in general with the typical gill-pouch, and a smaller dorsal portion (Fig. 130, B). The former is transitory and disappears without becoming perforated, while the latter, which is perforated for a short time only, enlarges and becomes differentiated as a part of the middle ear or tympanic cavity. The major portion of this cavity is, however, derived from the cavity of the pharynx adjoining the dorsal portion of the hyomandibular pouch. This part of the pharynx becomes incompletely cut off from the remainder of the pharyngeal cavity by a horizontal shelf or partition, a narrow slit remaining open in the mid-line. The narrow pharyngeal space thus formed, and the dorsal portion of the hyomandibular pouch, enlarge distally, between the otocyst and the surface of the head, as the rudiment of the tympanic cavity; the narrow medial portion of the pharyngeal space becomes the Eustachian tubes, opening into the pharynx by the slit mentioned.
The mesenchyme of the dorsal wall of the tympanic cavity becomes differentiated into the two inner auditory ossicles. The cavity then extends dorsally around either border of this mesenchymal region, which is thus formed into a stalk containing the two ossicles and connecting the surface of the head with the wall of the otocyst (twelve days).
Meanwhile the external auditory meatus forms, as a depression on the surface of the head between the dorsal and ventral portions of the original hyomandibular pouch. This depression deepens and finally the tympanic cavity meets it; the membrane separating the two cavities does not perforate, but remains as the tympanic membrane or- ear-drum. In the interior of this membrane, the mesenchyme which remains between its outer ectodermal and inner endodermal layers, differentiates into the stapes, which comes into relation with the malleus and incus, already marked out in the mesenchymatous rod crossing the tympanic cavity.
The Olfactory Organ
This develops much later than the eye and ear, a fact which is possibly correlated with the secondary importance of the olfactory sense in the birds. Its appearance is made at the close of the second day, as a pair of circular thickenings in the superficial ectoderm just anterior to the eyes. These thickenings are due to the elongation of the epithelial cells and mark the primary differentiation of the olfactory epithelium. Each patch soon becomes invaginated, forming an olfactory pit, which remains open to the surface of the head. Outgrowth of the fore-brain produces an apparent shifting of the external openings of the olfactory pits to the ventro-lateral surfaces of the head in the margin of the stomodaBum. The two pits are separated by a broad ridge, produced by the enlargement of the fore- brain; this is the fronto-nasal process. The outer border of the opening of the olfactory pit also becomes elevated, and about the fifth day becomes joined with the fronto-nasal process by a bridge of tissue, extending across the olfactory opening and dividing it into upper and lower portions. This bridge enlarges as the rudiment of a part of the upper jaw, and the two openings thus have quite different fates. The upper is carried outward and upward and forms the external nares; the lower is carried downward and inward (relatively) as the internal nares (choance).
The olfactory pit has already begun to deepen before the division of its external aperture. The true olfactory epithelium, which is distinguished from the adjacent non-sensory epithelium by the fact that the former remains only one cell thick, is limited to the deeper part of the pit, so that the olfactory and respiratory portions of the olfactory chamber are sharply distinguished even in these early stages. During the fourth to eighth days, the internal nares are carried farther back by the development of the palate, and the three pairs of turbinates make their appearance, growing in from the outer or lateral wall of the chamber. The lower turbinate extends into the respiratory portion, the middle and upper turbinates into the olfactory portion; later, however, the epithelium covering the middle turbinate loses its olfactory character and becomes like that of the respiratory part.
The true olfactory epithelium contains neuroblasts as well as ordinary epithelial cells. Superficially the former send out to, or above, the surface of the epithelium, short processes which are sensory or receptive in character. These same cells send out also long processes (axons) which grow into the wall of the adjacent telencephalon and form the true olfactory nerves. The sensory epithelium of the olfactory organ is therefore a neuro-epithelium. The I cranial nerve called the olfactory, is composed of these fibers.
The Alimentary Tract And Its Appendages
We have already described the formation of the main divisions of the embryonic gut; these are the fore-gut, with which we described the pharynx and oral plate, the hind-gut with the postanal gut, and the mid-gut connecting with the splanchnic stalk. We shall now review the early development of the various regions of the tract and of the appendages or derivatives of each portion.
Organs of the Fore-gut=
We left the fore-gut, at the thirtieth hour, as the short but wide cavity of the head-fold, extending from the oral plate to the anterior intestinal portal (Fig. 99). Later we have seen that, through the process of folding the embryo off the yolk, the splanchnopleural gut is rapidly extended posteriorly from the fore-gut and anteriorly from the hind-gut, and is closed in entirely, save where it communicates with the yolk-sac by way of the splanchnic stalk. That part of the gut which is thus formed primarily by the approach of the lateral embryonic folds is distinguished as the mid-gut, the definitive fore- and hindgut being formed primarily by the head- and tail-folds. Embryologically the fore- and hind-gut are more important than the mid-gut, for in connection with these regions develop all of the important appendages of the alimentary tract.
In connection with the fore-gut we have to describe the formation of the pharynx and visceral arches and pouches, the thyroid, the thymus and post-branchial bodies, the whole respiratory tract, the oesophagus and stomach, the liver, and the pancreas; in addition we must include the stomodseum and the structures derived from it, the hypophysis and the organs of the buccal cavity.
The stomodceum is an ectodermally lined depression on the lower side of the head; the oral plate is at its bottom (Figs. 99, 123, A). The depth of the stomodaeum is increased by the formation and growth of the jaws. As previously noted, the oral plate becomes perforated during the third day and then gradually disappears, the stomodaeum itself, however, is the seat of several important organs. The hypophysis appears about the forty-fourth hour, as an elongated evagination from its mid-dorsal wall, just in front of the oral plate (Fig. 123). It grows directly toward the ventral surface of the diencephalon, in the region of the infundibulum, which it reaches at about the beginning of the third day. Later it becomes glandular, loses its connection with the epithelium of the stomodaeum and joins with the infundibulum to form the glandular portion of the pituitary body.
The cavity of the stomodaeum and the future buccal cavity are practically coincident, whether precisely or not can hardly be said, on account of the disappearance of the oral plate before the formation of any other landmark. The maxillary and mandibular arches, whose formation is described below, extend forward, around the sides of the stomodaeum forming the rudiments of the jaws; the buccal cavity is considerably enlarged by their formation and their enlargement as the beak. An incomplete palate is formed later, above which the pharyngeal cavity extends. On the upper surface of the beak is formed a superficial horny egg-tooth, which is used in perforating the shell and shell membrane at the close of incubation; and on the margins of the jaws slight, transitory ridges appear, representing the vestiges of the enamel organ all that there is left of the true teeth of other vertebrates. Although the tongue extends forward into the buccal cavity, it is really a pharyngeal derivative.
The pharynx is the most complicated region of the embryonic gut. On account of the obliquity of the oral plate, the antero-dorsal portion of the pharynx may be described as pre-oral; this region is known as SeesseWs pouch, but when the oral plate disappears this is indistinguishable (Figs. 123, A; 130). We have already described, in connection with the ear, the separation of this antero-dorsal portion of the pharynx as the rudiment of a part of the tympanic cavity and the Eustachian tubes, which open into the pharynx through a median fissure in the palate, the tubal fissure.
Beginning the second day there grow out from the walls of the wide pharynx toward the surface of the head, a series of paired, vertically elongated pouches, the visceral pouches (Fig. 130). Of these there are four pairs, diminishing in size and importance posteriorly. The first and largest is the hyomandibular pouch, the other three are the branchial or gill-pouches, the last of which is very feebly developed. These visceral pouches, containing extensions of the pharyngeal cavity, push out to the surface ectoderm with which they fuse intimately, dividing the body wall of the region into a series of vertical sections between them; these are the visceral arches. The visceral arches are composed chiefly of mesenchyme, in which develop later the aortic arches and the cartilaginous visceral arches; each is covered externally by ectoderm, and internally and laterally by endoderm. Five visceral arches are thus marked out. The first is in front of the hyomandibular pouch, between this and the mouth, and is known as the mandibular arch. The second, or hyoid arch, lies between the hyomandibular and the second visceral pouches, while the remaining three branchial arches (third to fifth visceral arches) lie posterior to the second, third, and fourth visceral pouches. Like the pouches these diminish in size and importance posteriorly, the last (fifth) being only a slight and transitory vestige.
Fig. 130. Models of the pharynx and associated structures in the chick. After Kastchenko. A. Ventro-lateral view of pharynx at the beginning of the third day. B. Lateral view of the pharynx and associated nervous and vascular structures, at the end of the third day. Nervous structures are left unshaded; arteries in solid black; veins lightly stippled; pharyngeal structures darkly stippled, a. Auditory sac; aa, aortic arches; ao, dorsal aorta; cf, choroid fissure; cv, posterior cardinal vein; dC, ductus Cuvieri; ej, external jugular vein; gV, Gasserian ganglion of V cranial nerve; gVII, geniculate ganglion of VII cranial nerve; gVIII, acustic ganglion of VIII cranial nerve; glX, ganglion petrosum of IX cranial nerve; gX, ganglion nodosum of X cranial nerve; h, hypophysis; ic, internal carotid artery; j, internal jugular vein; I, rudiment of larynx; o, oral evagination of fore-gut; oe,oesophagus; op, optic vesicle enclosing lens; p, pulmonary artery; pIX, placode of IX cranial nerve; pX, placode of X cranial nerve; s, stomach; S, Seessel's pocket (preoral gut); st, stomodaeum; t, rudiment of trachea; 1-4, first to fourth visceral pouches (or their ventral portions, in B) ; Id, 2d, dorsal portions of first and second visceral pouches; IX, glossopharyngeal nerve; X, vagus nerve; XI, hypoglossal nerve.
The vertical fusions of ectoderm and endoderm along the outer borders of the visceral pouches are interrupted just below the upper ends of the pouches, so that dorsal and ventral portions of each fusion are to be distinguished (Fig. 130, B). The surface of the head becomes depressed in the lines of fusion, so that a series of vertical grooves marks externally the disposition of the visceral arches and pouches.
The second visceral pouch (first branchial) is the best developed, and about the end of the second day both upper and lower fusions are perforated as the vestiges of a gill cleft; these perforations close during the fourth day without leaving any trace. In the third pouch a gill cleft is similarly formed and closed a little later. In the first pouch (hyomandibular) only the dorsal fusion is perforated (spiracular cleft) shortly before the perforation of the second pouch. No cleft appears in the fourth pouch, only the dorsal portion of which fuses with the ectoderm.
After the fourth day the visceral pouches become reduced. The first undergoes a change in function and takes an essential part in the formation of the tympanic cavity, as described above. For the most part the other visceral pouches finally disappear, but from parts of their epithelial walls the thymus and the post-branchial bodies are derived. The thymus is chiefly derived from part of the dorsal epithelium of the third visceral pouch, but the fourth contributes to a small extent. A transitory anterior portion of the thymus is derived from the epithelium of the second pouch. The thymus becomes a very considerable embryonic structure, extending finally throughout the neck region. The post-branchial bodies are epithelial buds connected with the fourth visceral pouches, They are to be regarded as vestiges of a fifth pair of visceral pouches and are thus serially homologous with the thymus elements (Fig. 131).
The thyroid body also arises in connection with this part of the pharynx. This appears during the middle of the second day as a thickened patch of cells in the floor of the pharynx, between the lower ends of the second visceral pouches. This plate of cells evaginates toward the close of the second day (Fig. 123), and soon appears as an entirely closed sac below the pharynx. Later (seventh day) it divides into a pair of vesicles which enlarge and migrate a short distance posteriorly.
Fig. 131. Derivatives of the visceral pouches and associated organs, in the chick. From Lillie (Development of the Chick). After Verdun (Maurer). Combined from frontal sections. A. In embryo of seven days. B. In embryo of eight days. Ep.3, EpA. Epithelioid bodies derived from third and fourth visceral pouches; J, jugular vein; p'br., p'br. (V)., postbranchial bodies derived from fifth visceral pouch; Ph., pharynx; Th.3., ThA., thymus bodies derived from third and fourth visceral pouches; T'r., thyroid body; ///, IV, third and fourth visceral clefts.
Finally we must describe, as an appendage of the pharynx, the pulmonary tract. For a short distance behind the branchial region the pharynx becomes narrower and is deepened by the formation, late the second day, of a ventral groove (Fig. 130, A). This groove is the beginning of the whole pulmonary system. The depression becomes well marked early the third day as the laryhgo-tracheal groove, and its posterior end expands transversely forming the rudiments of the lungs. The groove then becomes cut off from the pharyngeal cavity as 'the rudiment of the trachea, remaining open out of the pharynx only at its anterior end; this opening is the glottis, behind which the larynx develops later. From the eighth to the eleventh days the glottis and larynx are obstructed by a cell mass, and the glottis itself remains closed for some time longer.
Just in front of the glottis, in fact both immediately behind and in front of the thyroid rudiment, the floor of the pharynx is elevated (fourth day), the two papillae thus formed representing the beginning of the tongue. As these rudiments enlarge they fuse together, the thyroid having been cut off meanwhile, and grow forward into the buccal cavity, finally extending nearly to the tip of the jaws.
The bifurcated posterior extremity of the laryngo-tracheal groove or lung rudiment, grows backward through the surroupding mesenchyme; the tubes thus formed are the rudiments of the bronchi. By a sort of budding process they form the bronchioles and terminal alveoli of the lung proper. The mesodermal parts of the entire pulmonary tract are derived from the splanchnic mesoderm of the primary gut-wall. The air-sacs are also formed from terminal dilations of branches of the bronchial tubes.
Passing backward from the pharynx the gut is considerably narrowed for a short distance as the cesophagus, but it soon expands again as the rudiment of the stomach (third day). Before these organs are differentiated, however, the liver appears. This makes its appearance toward the close of the second day, in the region where the fore-gut is at that time open by the anterior intestinal portal, i.e., just back of the future posterior limit of the stomach. Here two evaginations of the ventral wall of the gut, or portal, push out, one above the other in the mid-line ; they extend forward as pouch-like outgrowths, through the mesoderm of the ventral mesentery, below the stomach region. This is the region where the great veins are converging toward the heart (ductus venosus, ductus Cuvieri, see below). The anterior liver diverticulum appears some hours before the posterior, and as it grows forward it lies to the left, the later posterior diverticulum then extends rather toward the right side, and although it becomes the larger, it does not grow as far forward as the anterior diverticulum. During the third and fourth days both diverticula branch and anastomose, forming a network of liver tissue (Fig. 123, B) around the large vein (ductus venosus). The liver soon enlarges enormously and early becomes very vascular, through the development of vessels connecting with the ductus venosus, directly among the meshes of the liver substance.
The bile duct and gall-bladder arise from the short ventral region of the gut between the two liver diverticula; this region grows out carrying with it the openings of the diverticula, which thus come to open into a common chamber, the ductus choledochus or common bile duct. The gall-bladder develops in connection with the duct of the posterior liver diverticulum. The common bile duct is a transitory structure, and when it disappears the two liver (bile) ducts again open separately into the gut.
About the same time and in the same general region as the liver, the pancreas develops, from three separate diverticula. A dorsal median diverticulum grows out, directly opposite the posterior liver diverticulum, about the end of the third day. Right and left ventral pancreatic diverticula appear later, pushing out from the walls of the ductus choledochus close to the gutwall. When the ductus choledochus disappears these pancreatic rudiments open separately into the gut. As these diverticula enlarge they branch distally and by a budding process form the glandular units of the organ. The bodies of the three rudiments finally join, forming a common gland, although their ducts remain opening separately near the two bile ducts.
Organs of the Hind-gut
Embryologically the most important appendage of the hindgut is the allantois. In describing the formation of this organ we mentioned the essential steps in the establishment of the hind-gut itself, and described the formation of the postanal gut and the beginning of the cloaca (Figs. 120, 121). On the ventral side of the hind-gut, between the outgrowing allantois and the base of the tail the ectoderm becomes pitted in toward the cloaca forming the proctodceum. The ectodermal epithelium of the proctodaeum fuses with the endodermal lining of the cloaca forming the anal plate. This was originally toward the dorsal surface of the embryo, but was pushed into a ventral position by the formation and growth of the tail-bud (Fig. 121).
The cloaca becomes a deep but narrow cavity; it receives, antero-dorsally, the opening of the terminal portion of the intestine, and the allantoic stalk connects antero-ventrally. Laterally, either side of the rectal opening, the urinogenital ducts discharge into the cloaca. During the fifth and sixth days the postero-ventral portion of the cloaca is temporarily closed by the fusion of its walls. The cavity which re-forms here is the rudiment of the bursa Fabricii, which acquires an opening directly into the proctodseum just outside the anal plate. Thus the embryonic cloaca gives rise chiefly to that part of the adult cloaca into which the urinary and genital ducts open. The anal plate finally becomes perforated early in the third week of incubation.
The embryonic mid-gut gives rise to the intestinal tract extending from the hepatic and pancreatic diverticula to the cloaca. Its establishment through the approach and fusion of the lateral splanchnopleural folds has been described in the preceding chapter. 'It remains open by the splanchnic stalk to the yolk-sac until toward the close of the embryonic period (see above).
Although really derived from the embryonic fore-gut, we may include here certain details in the later development of of the oesophagus and stomach, the formation of which was mentioned above. The stomach and intestine extend through the body cavity, from the dorsal wall of which they are suspended by a double mesodermal fold, the dorsal mesentery and mesogastrium, which represents the original dorsal fusion of the lateral splanchnopleural folds involved in the establishment of the intestinal groove and tube. The similarly formed ventral mesentery disappears immediately after its formation, save in the region of the stomach and liver, where it forms the gastrohepatic ligament.
Fig. 132. Partially dissected viscera of the chick, from the right side. After Duval. A. Of a six-day chick, enlarged slightly less than six times. B. Of a thirteen day chick, enlarged two and one-half times, showing the elongated intestine and its extension into the umbilical stalk, a, Right auricle; aZ, allantois; as, abdominal air sac; 6, bulbus arteriosus; c, caecal processes; d, loop of duodenum; dj, duodenal-jejunal flexure (a relatively fixed point during the elongation of the intestine) ; /, fore-limb bud (cut through) ; g, gizzard; go, gonad ; A, hind-limb bud (cut through) ; i, loops of small intestine; I, liver; Ig, lung; II, left lobe of liver; h, left ventricle; M, rudiment of Miillerian duct (tubal ridge) ; p, pancreas; r, rectum; rl, right lobe of liver; rv, right ventricle; s, yolk stalk; u, umbilical stalk; W, Wolffian body or mesonephros.
The oesophagus elongates with the neck, and during the seventh to eleventh days is closed just back of the glottis by cells proliferated from its wall. The crop appears as a posterior dilation of the oesophagus just in front of the stomach. During the fifth to seventh days the enlarging stomach becomes differentiated into the anterior proventriculus, with thick glandular walls, and the posterior gizzard, with its thick muscular coats. The horny lining of the gizzard is derived from the secretion of specific glands in its own wall.
Beginning the third or fourth day of incubation the mid-gut, including the stomach, commences to elongate, and as a result the tract becomes first simply looped, and then complexly folded (Fig. 132). First the stomach bends to the right, returning to the median region near its opening into the intestine. The first section of the intestine is the duodenum; this is a very short section, receiving the ducts of the liver and pancreas. The duodenum elongates very little and remains as a relatively fixed region, closely attached to the dorsal body wall. Similarly the terminal portion of the intestine, the rectum and large intestine, elongates only slightly. Between the duodenum and the large intestine the jejunum or vitelline portion of the small intestine elongates considerably, and is consequently thrown first into an S-shape. The yolk-sac connects with the apex of the lower loop (Fig. 132). Later this whole section shows secondary loops or twistings along each primary loop. At the connection of the small and large intestines the two intestinal cceca grow out during the second week.
The Vascular System
The formation of the vascular system and its development up to the thirtieth hour, we have already described; and we have also mentioned the important steps in the development of the extra-embryonic circulation (yolk-sac and allantois). We must now trace the important steps in the development of the true embryonic circulation, from the stage where we left it. Let us recall that we left the heart as a bent tube, suspended in the pericardial cavity; anteriorly it leads, by way of the first or mandibular pair of aortic arches, into the dorsal aorta, the chief branches of which (vitelline arteries) supply the extraembryonic organs. The embryonic venous system at that time consisted only of the roots of the vitelline veins, returning the blood from the yolk-sac and opening directly into the posterior end of the heart. The main vessels of the yolk-sac and allantois are described in the preceding chapter, and we shall need to add little to those accounts of the extra-embryonic circulation.
The sharp bending of the heart to the right divides it roughly into anterior and posterior limbs (Fig. 133, A), and as it continues to elongate an additional loop appears, directed posteriorly from near the apex of the original loop. The entire structure then swings underneath the pharynx and the loops become less widely spread out (Fig. 133, B). The extent of the heart is increased posteriorly by the addition of a region formed by the fusion of the roots of the paired lateral vitelline or omphalomesenteric veins; the chamber thus formed is the sinus venosu's. .
During the third day certain constrictions appear, dividing the tube intd its primary chambers, and each of these shows characteristic modifications in form, so that by the end of the third day the following regions are distinctly marked. The sinus venosus } formed by the confluence of the omphalomesenteric veins, is a wide triangular fcvity with thin walls; it receives also the embryonic veins, the duefrus venosus and the paired ductus Cuvieri (see below). Its a^ex is anterior, where it opens into the atrium or auricle bythe sinu-auricular aperture; this opens into the postero-dorsal region of the auricle. The auricle is formed from the originally posterior loop of the heart tube, now dorsal in position. The auricle already shows signs of its future division in that it is laterally expanded; the sinus venosus is more directly connected with its right side and its left side extends forward nearly to the limit of the pericardial cavity. The wall of the auricle remains thin like that of the sinus venosus; its cavity opens downward into the dorsal region of the ventricle.
The ventricle is formed essentially from the secondary posterior loop of the heart tube, and is now separated from the auricle by the narrowed auriculo-ventricular aperture (Fig. 133)., The ventricle occupies the ventral region of the pericardial cavity beneath the auricle. The walls are already thickened and spongy. Anteriorly a slight constriction separates the ventricle -from the bulbus arteriosus, the most anterior chamber of the heart, formed from the anterior loop of the original heart tube and now passing obliquely upward to the antero-dorsal wall of the pericardial cavity, where it connects with the truncus arteriosus in the floor of the pharynx. The wall of the bulbus is also much thickened at this time.
Fig. 133. The development in the heart of the chick. A, F, after Hochstetter; B-E, after Greil. A-E, ventral views of the heart; A, of a forty-hour embryo; B, of a 2.1 mm. embryo; C, of a 3.0 mm. embryo; D, of a 5.0 mm. embryo; E, of a 6.5 mm. embryo. F. Frontal section through the heart of a 9 mm. embryo, a, Auricle; b, bulbus; d, roots of dorsal aorta; e, median endothelial cushion; i, interventricular groove; la, left auricle; le, lateral endothelial cushion; lv, left ventricle; om, vitelline artery; p, left pulmonary artery; ra, right auricle; rv, right ventricle; s, interventricular septum, sa, interauricular septum; t, roots of aortic arches; v, ventricle.
Long before the end of the third day the heart is beating regularly and rapidly. Its first irregular twitching begins toward the middle of the second day and before the end of this day its contraction becomes quite regular.
The later development of the heart may be sketched only roughly. There are further changes in the position of the heart, as the net result of which the ventricle assumes a posterior, and the auricles an antero-dorsal, location; the auricles also grow ventrally around the bulbus, which finally occupies a median ventral position.
The bulbus arteriosus finally loses its identity as a separate chamber. Three semilunar valves develop, about in its middle, and its anterior section then becomes transformed into the proximal parts of the truncus arteriosus (finally the root of the dorsal aorta) and the pulmonary artery, while its posterior section is absorbed into the ventricles. Similarly the sinus venosus becomes incorporated into the right auricle, and the sinu-auricular valves, which had developed from the wall of the sinuauricular aperture, entirely disappear. Thus of the original four chambers of the heart only two remain separate. The cavities of these two chambers, the auricle and ventricle, then become secondarily divided longitudinally, so that the heart may again be described as four-parted, though in a very different sense.
From the postero-dorsal wall of the auricle, between the openings of the sinus venosus and the pulmonary vein (see below) a thin partition grows downward and forward, during the fourth day, and soon reaches a thickened cushion of cells lying on the upper and lower sides of the auriculo-ventricular aperture, thus completely dividing the primary auricular cavity into right and left cavities (Fig. 133, F). This interauricular septum early becomes fenestrated and is not completely re-formed until after hatching. At the same time the ventricle is becoming divided into right and left portions by an interventricular septum. This commences as an extension of the spongy wall of the ventricle near its posterior apex; it becomes a thick partition, rapidly extends anteriorly, meeting and fusing with the cushion of the' auriculo- ventricular aperture, with which the interauricular septum has already connected. Finally the division of the ventricle is completed save for a small antero- ventral aperture, the interventricular foramen, by which the root of the dorsal aorta later connects with the left ventricle.
The bulbus arteriosus too becomes divided before its fusion with th3 ventricle, by a partition extending from the anterior margin of the pulmonary aortic arch (see below) back to the ventricles. The effect of this is to connect the pulmonary aortic arches with the right ventricle and the systemic aortic arch with the left ventricle. When this bulbus region is absorbed, as described above, the pulmonary arteries and the dorsal aorta arise directly from the right and left ventricles, respectively, and the separate blood streams are established.
The Aortic Arches and the Arterial System
At the thirtieth hour the heart is connected with the dorsal aorta by a single pair of aortic arches running through the first or mandibular visceral arch. Later an aortic arch forms in each visceral arch, connecting the truncus arteriosus or ventral aorta with the lateral dorsal aortas. The second or hyoid aortic arch forms during the latter part of the second day and at the end of that day the third aortic arch is completed. The fourth is formed by the end of the third day and during the fourth and fifth days fifth and sixth aortic arches are formed in the tissues posterior to the last (fourth) visceral pouch (Fig. 134, A ) . Of these arches the fourth and sixth are the best developed, while the fifth is present only as a transitory and incompletely developed vestige.
This embryonic aortic arch system is converted into the adult condition chiefly by a series of degenerations. During the third and fourth days the first (mandibular) and second (hyoid) arches disappear, leaving only their continuous ventral roots as the root of the external carotid artery. The lateral dorsal aortaB have meanwhile continued forward, as the internal carotid arteries, supplying the brain and other organs of the head. These parts of the lateral dorsal aortae become separated, during the sixth and seventh days from the remainder of the lateral dorsal aortse by an interruption in these vessels just back of the dorsal attachment of the third aortic arch; thus the internal carotid arteries arise only from the third aortic arch, which is consequently known as the carotid arch (Fig. 134, B). The ventral roots of the first and second arches (external carotids) remain as branches from the bases of the carotid arch (roots of the third arches), supplying the mandibular region.
Fig. 134. Aortic arches of the chick. From Lillie (Development of the Chick), A, after Locy. A. Of the left side of a chick of four and one-half days; from an injection. B. Reconstruction from sagittal sections of an eight-day embryo. Ao. A. Arch of the aorta (systemic arch) ; A.o.m., vitelline artery; Car., carotid artery; Car. ext., external carotid artery; Car. int., internal carotid artery; D.a., ductus arteriosus; d.Ao., dorsal aorta; p.A., pulmonary artery; S'cL, subclavian artery; 3-6, third to sixth aortic arches (first to fourth branchial aortic arches).
The fourth, or systemic arch, is at first symmetrically developed like the others, but during the fifth and sixth days it becomes reduced on the left side and correspondingly enlarged on the right. Finally the left systemic arch wholly disappears, and the anterior part of the left division of the truncus remains only as the stem of the left carotid artery. Meanwhile, it will be recalled, the right side of the truncus has connected with the left ventricle alone, so that the blood from this side of the heart is now carried by the third arches to the carotids, and by the right systemic or fourth arch to the general dorsal aorta.
The fifth aortic arches having already disappeared, .only the sixth is left connecting now with the right ventricle. The sixth arches ultimately form the roots of the pulmonary arteries,
but throughout embryonic life they remain, on each side connected with the roots of the definitive dorsal aorta. The true pulmonary arteries are small vessels passing backward from the upper ends of the sixth or pulmonary arches (Fig. 134). That part of each arch between the origin of the pulmonary artery and the dorsal aorta is known as the ductus Botalli, and shortly after hatching the two ductus Botalli become closed as strands of connective tissue, turning the whole of the blood stream of these leaves the dorsal aorta connected with the heart only by the right systemic arch (Fig. 135).
Fig. 135. The heart and aortic arches flrr V,p S rominp 1 from the of a chick embryo the latter part of the sixth day. From a dissection. From right side of the heart, into Lillie (Development of the Chick) after Sabin. Au. Auricles; Car. com., common tne pulmonary arteries, carotid artery; S'cl.d., S.cl.s., primary and Thereupon the dorsal resecondary subclavian arteries; 3, 4, 6, third L (carotid), fourth (systemic), and sixth mainder of the left lateral (pulmonary) aortic arches. dorgal ^^ disappears and
Certain branches of the aortic arches and dorsal aorta deserve a special word. The dorsal aorta gives off segment al branches between the somites, known as the segmental arteries (Fig. 109, B). Some of these become enlarged as the roots of the arteries supplying the limbs, the subclavian and sciatic arteries. A branch from the carotid artery grows out and connects with the subclavian, finally forming its true root, its original root from the aorta disappearing about the ninth day. The sciatic artery gives off branches, the umbilical arteries, supplying the allantois; the right umbilical artery is the smaller and finally disappears.
During embryonic life the chief branches of the dorsal aorta, and really those first formed, are the pair of large omphalomesenteric or vitelline arteries, distributed to the yolk-sac by way of the splanchnic stalk. The proximal parts of these become fused as a single vessel from the base of which is derived the anterior mesenteric artery. The posterior mesenteric and coeliac arteries are derived directly from the dorsal aorta. The dorsal aorta also gives off a series of small twigs supplying the excretory organs, certain of which enlarge forming the renal and genital arteries (Fig. 138).
The Venous System
We have thus far described only the veins of the extraembryonic circulation, for at the thirtieth hour the embryonic veins are not developed. It will not be necessary to add anything regarding the strictly extra-embryonic portions of these vessels, but their intra-embryonic terminations take an important part in the formation of the definitive embryonic circulation.
The first embryonic veins to appear, about the middle and latter part of the second day, are the anterior cardinal veins. Coming from the brain they extend along its ventro-lateral walls, beneath the auditory sacs, receiving as they pass, branches from the general head region, including the three anterior somites. Just back of the head they also receive later, branches from the floor of the pharynx (external jugular veins); the anterior cardinals themselves become known as the internal jugular veins. The proximal parts of the anterior cardinal veins are considerably enlarged as the ductus Cuvieri, which turn inward and downward and pass into the sinus venosus (Fig. 137).
From the upper end of each ductus Cuvieri an outgrowth extends posteriorly as the rudiment of the posterior cardinal vein, which passes along the Wolffian duct (see below), finally reaching nearly to the base of the tail. The posterior cardinal veins receive the intersomitic or intersegmental veins, except the first three, and the vessels of the nephros (mesonephros, see below). The veins of the fore-limbs also discharge into the posterior cardinals near the ductus Cuvieri. The anterior and posterior cardinal veins are consequently the chief somatic veins of the early embryo, and it should be noted that all of the somatic veins connect with the heart by way of the ductus Cuvieri.
The splanchnic veins of the digestive tract and its appendages are primarily related with the intra-embryonic portions of the great veins of the yol-sac, the omphalomesenteric veins. We have already seen how the proximal ends of these veins unite to form the sinus venosus; they continue to fuse posterior to the sinus venosus, and form thus the ductus venosus, around which, as we have seen, the liver develops. The ductus venosus and the ductus Cuvieri are the only vessels emptying directly into the heart, until the time when the pulmonary veins appear. The omphalomesenteric veins, entering the embryo, pass across the body cavity to the mid-line, beneath the gut and between the two liver diverticula.
It should be noted here that between each omphalomesenteric vein and the dorsal body wall an extensive fusion occurs, forming an incomplete oblique partition through that part of the body cavity immediately posterior to the heart. These fusions are known as the lateral mesocardia, and they are of considerable importance in the later history of the cavities of the body (Fig. 139). The ductus Cuvieri pass from the dorsal body wall to the sinus venosus through the anterior parts of the lateral mesocardia.
Posterior to the ductus venosus the two omDhalomesenteric or lateral vitelline veins anastomose, at about the age of three days, on the dorsal side of the intestine, posterior to the pancreatic rudiment (Fig. 136). Thereupon the base of the left vein rapidly disappears, so that during the fourth day all of the blood from the yolk-sac is returned to the heart by the right vein, for it will be recalled that the original or anterior vitelline veins have previously fused and connected with the right omphalomesenteric vein; and now a large vein coming directly from the posterior part of the yolk-sac similarly opens into the same trunk.
Fig. 136. Diagrams illustrating the formation of the omphalomesenteric and umbilical veins, in the chick. After Hochstetter. A. At about fifty-eight hours. B. At about sixty-five hours. Veins joined dorsal to the gut. C. At about seventy-five hours. Veins again separate. D. At about eighty hours. Secondary union of veins around the gut. E. At about one hundred hours. Definitive arrangement of the vessels, c. Vena cava posterior (inferior) ; dC, ductus Cuvieri; dv, ductus venosus; g, gut; hi, left hepatic vein; hr, right hepatic vein; Z, liver; o, omphalo-mesenteric vein; p, anterior intestinal portal ; pa, rudiment of pancreas; ul, left umbilical vein; ur, right umbilical vein; v, vitelline vein; I, II, primary and secondary venous rings around the gut.
By the end of the fourth day the two omphalomesenteric veins again anastomose still farther back, and now the intermediate portion of the right vein disappears. The embryonic course of the omphalomesenteric veins may therefore be described as follows (Fig. 136) ; they enter the body symmetrically, passing directly to the ventral side of the intestine just in front of the anterior intestinal portal; here they fuse into a single vessel which passes anteriorly around the left side of the intestine to its dorsal surface and thence across to the right side, where it enters the liver.
This portion of the omphalomesenteric vein becomes the trunk of the hepatic portal vein in the following manner. As the vein passes through the liver to the ductus venosus, which is now embedded in it, it branches abundantly supplying the vascular spaces of the liver tissue, and soon the strands of liver cells push into the large vessel so that it becomes entirely broken up into small vessels and capillaries in the liver. The ductus venosus then remains as the efferent vessel, or hepatic vein, while the base of the omphalomesenteric vein itself be comes the afferent hepatic vessel, the hepatic portal vein. This arrangement is practically completed during the sixth day. Before this time the veins of the digestive tract appear; these collect into the mesenteric vein, which becomes the chief branch of the hepatic portal. A typical subintestinal vein is indicated the fourth day, coming from the tail and connecting with the left omphalomesenteric vein; it soon disappears without taking an essential part in the formation of any permanent venous structure.
Veins of considerable phyletic importance are the umbilical veins, which represent the lateral veins of the Elasmobranchs and the abdominal vein of the Amphibia. These appear early in the body wall, primarily as the veins of the limb-buds, opening into the ductus Cuvieri (Fig. 137). During the fourth day they connect with the veins of the allantois, and shortly there after the right vein disappears, while proximally the connection of the left vein with the ductus Cuvieri is lost, and this vessel acquires a new connection with the intra-hepatic vessels and ductus venosus. Through this pathway the veins of the allantois then connect with the embryonic circulation.
The largest venous trunk of the fowl is the inferior vena cava or postcaval vein. As in other forms, this vein is in part an independent formation, and in part formed from the posterior cardinal system. The first part of the vena cava appears during the fourth day as a posterior outgrowth of the ductus venosus, which connects with a series of venous spaces in the dorsal wall of the liver, on the right side (Fig. 136). Soon this vein connects with the right posterior cardinal vein. The posterior cardinal veins pass along the dorsal side of the kidneys (mesonephroi, see below) receiving their vessels. But during the fourth day a system of venous spaces appears on the ventral side of the kidney; these vessels are known as the subcardinal veins (Fig. 138). During the sixth day the inferior vena cava connects with the right subcardinal vein, the two subcardinal veins anastomose posterior to this connection, and the anterior parts of both posterior cardinal veins disappear. The net result of these changes is that the hinder parts of the posterior cardinals form the afferent renal trunks or renal portal veins, the subcardinals form the efferent renal vessels leading into the inferior vena cava, through which all of the blood from the embryonic kidneys (mesonephroi) is returned directly to the heart. This arrangement continues until this embryonic kidney is replaced by the definitive kidney of the adult (metanephros), when the posterior cardinal veins, then the renal veins, connect directly with the subcardinal veins and the vena cava, and the renal portal system disappears. The subclavian veins which originally opened into the proximal parts of the posterior cardinals, acquire openings into the ductus Cuvieri near the vertebral and external jugular veins.
Fig. 137. Injected chick embryo of the third day, showing the arrangement of the cardinal veins and the formation of the umbilical vein from capillary networks. From Evans. A.C.V., Anterior cardinal vein; P.C.V., posterior cardinal vein; U.V., umbilical vein.
Fig. 138. Diagrammatic lateral view of the chief embryonic blood-vessels of the chick, during the sixth day. After Lillie. a. Auricle; al, allantoic stalk; ao, dorsal aorta; c, cceliac artery; ca, caudal artery; cl, cloaca; cv, caudal vein; da, ductus arteriosus; dv, ductus venosus; ec, external carotid artery; ej, external jugular vein; i, intestine; ic, internal carotid artery; ij, internal jugular vein; I, liver; ra, mesonephros; ma, mesenteric artery; mv, mesenteric vein; p, pulmonary artery; pc, posterior cardinal vein; pv, pulmonary vein; s, sciatic artery; sc, subclavian artery; SCT, subclavian vein; st, yolk-stalk; sv, subcardinal vein; ul, left umbilical artery; ur, right umbilical artery; uv, left umbilical vein; v, ventricle; va, vitelline artery; vca, anterior vena cava (anterior cardinal vein); vp, posterior vena cava; vv, vitelline vein; y, yolk-sac; 3, 4, 6, third, fourth, and sixth aortic arches.
The Lymphatic System and Spleen
The development of the lymphatic system is imperfectly known in the chick. A pair of anterior or cervical lymph hearts appears during the fifth day, and. from these lymphatic networks grow out extending posteriorly, parallel with the lateral veins of the body; by the eighth day these nets are developed into definite lymphatic vessels. A pair of posterior or caudal lymph hearts appears early the seventh day as a series of lateral outgrowths from the first five coccygeal veins (tributaries of the posterior cardinal veins). These branches anastomose with one another, forming an irregular sac or lymph heart, on each side, which remains connected with the second, third, and fourth coccygeal veins. The walls of the hearts become muscular and rhythmically contractile during the eighth and ninth days.
During the ninth day the posterior lymph hearts connect with a system of lymphatic spaces around the posterior section of the dorsal aorta, and this space connects in turn with the thoracic ducts. These lymphatic trunks are visible on the eighth day, when they are described as two solid strands of mesenchyme, extending from the thyroid body to the roots of the coeliac artery. They become hollowed out and connect with the ductus Botalli, the dorsal aorta and the ductus Cuvieri. These canals then approach and fuse, and about the twelfth day connect with the posterior lymph hearts by way of the lymphatic vessel around the posterior dorsal aorta. (It is entirely probable that the connections between the thoracic ducts and the blood-vessels represent the primarily formative outgrowths of the ducts from the vascular endothelium, from which the cords have extended and fused secondarily, but direct observations to this effect are wanting.)
The anterior lymphatic hearts apparently disappear early. The posterior lymph hearts attain their maximum development during the fourteenth and fifteenth days, when they begin to retrogress and disappear entirely ten to fourteen days after hatching.
The spleen arises, during the fourth day, from a proliferation of peritoneal cells in the base of the mesentery just above the pancreatic region. It enlarges rapidly through continued cell proliferation and the accumulation of a mesenchymatous stroma. Its spaces, without definite endothelial walls, are directly continuous with the sinusoidal origins of its efferent vein, and from these spaces splenic cells enter the blood stream and become converted into blood corpuscles.
The Cavities Of The Body
The folding-off of the embryo from the yolk completes the roughing-in of the body cavity. From the very beginning the general embryonic body cavity shows signs of the differentiation of the region surrounding the heart as the pericardial cavity. We have already traced the origin of this part of the ccelom, in describing the origin and formation of the heart. We have also seen how the body cavity proper is formed and closed, and how it is partially divided longitudinally by the dorsal mesentery. It remains now for us to consider the essential steps in the complete separation of the pericardial cavity and the further subdivision of the primary body cavity.
Throughout the early stages of development the pericardial cavity is only incompletely closed off from the body cavity, since it is only partly closed posteriorly by the mesoderm in the wall of the anterior intestinal portal, and the vessels which are entering the heart from the yolk-sac. The formation of the lateral mesocardia (see above) extends the separation of the, two cavities, but they still remain connected above and below this partition. The pericardial cavity soon becomes restricted to the median region of the body and the general body cavity then pushes forward along the sides of the pericardial cavity.
These antero-lateral extensions of the body cavity are the rudiments of the pleural cavity; they soon extend inward toward the median line, dorsally to the pericardial cavity with which, however, they still connect above the lateral mesocardia. The pericardial cavity still connects with the general body cavity beneath the lateral mesocardia (Fig. 139).
The complete closure of the pericardial cavity is begun during the fourth day, by the formation of the septum transversum. This partition is established by the formation of tissue connecting the lateral mesocardia dorsally
Fig. 139. Part of a transverse section through the lateral mesocardia of a chick with thirty-five pairs of somites (about and ventrallv or ventro- seventy-two hours). After Lillie. a, Auricle;
, acm, accessory mesentery; am, amnion; ao,
With the body dorsal aorta; ba, bulbus arteriosus; ch, cho
"U7i^'i j-V, ron; CD, posterior cardinal vein; dC, due While the septum tus ^ dwi> dorsal mesenter ' y . ; liver .
soon becomes Z, lateral mesocardium; pc, pericardial . cavity; pe, pulmo-enteric recess; pg, pleural Complete between pen- groove; s, stomach; OT, sinus venosus; vm,
cardial and body cavities, ventral mesenterv it remains for a time incomplete between pleural and body cavities. As the lungs begin to expand they push out into the pleural cavities, the walls of which supply the greater part of their mesodermal tissue. Finally the lungs extend posteriorly as well as laterally and as they reach the region of the septum transversum this gradually becomes completed (about the tenth day) as the pleuro-peritoneal membrane, closing off the pleural cavity from the body cavity proper or peritoneal cavity.
The Later History Of The Mesodermal Somites
In the chick of thirty hours we saw how the embryonic mesoderm is divided into three general regions, (a) the axial somites, (b) the intermediate cell mass or nephrotome, (c) the distal lateral plate, continuous with the extra-embryonic mesoderm (Fig. 102). We have already described the chief structures derived from the lateral plate the vascular system and the ccelom and its derivatives, and it remains now to describe the structures derived from the somites and intermediate cell mass.
The following table, quoted from Lillie (Development of the Chick, pp. 184-185) gives a resume of the general disposition of the somites.
"In an embryo of 42 somites (about ninety-six hours), the value of the somites as determined by their relations and subsequent history is as follows :
1 to 4. Cephalic; entering into the composition of the occipital region of the skull.
5 to 16. Prebrachial; i.e., entering into the region between the wing and the skull.
17 to 19. Brachial.
20 to 25. Between wing and leg.
26 to 32. Leg somites.
33 to 35. Region of cloaca.
36 to 42. Caudal.
" More somites are formed later, the maximum number recorded being 52 (see Keibel and Abraham, Normaltafeln). In an eight-day chick the number of somites is again about 42, including the four fused with the skull. Thus the ten somites formed last are again lost."
The somites, excepting those at each end of the series, have essentially a similar history, differing only in later details of development (Fig. 119). Each gives rise to three structures: (a) the musck plate or myotome, (b) the cutis plate or dermatome, (c) the sclerotome. The somites form as solid segmental cell masses; their superficial cells are arranged as a rather dense wall, epithelial in character, which encloses a loosely arranged central mass of mesenchymal nature. The densely arranged cells soon become limited to the dorsal and dorso-lateral regions of the somites. The dorsal portion, in particular the region toward the nerve cord, forms the rudiment of the myotome or muscle plate, while the dorso-lateral region gives rise to the cutis plate. In the more loosely arranged core, the formation of intercellular substance begins very early, producing a truly mesenchymatous structure. This part of the somite then extends over toward the notochord and nerve cord, as the rudiment of the sclerotome.
The myotome becomes thin and turns under the thicker cutis plate, finally extending downward and outward entirely beneath it, occupying a position between the spinal ganglion and the cutis plate. The cells of the myotome elongate anteroposteriorly, through the whole extent of the segment, and each becomes converted into a striated muscle fiber. Later the myotomes enlarge, as then- component cells multiply and grow, and each extends down into the body wall. Opposite the limbbuds, outgrowths of the myotomes extend into these, forming their musculature. The entire voluntary musculature of the chick develops from the myotomes; the involuntary musculature is mesenchymal in origin, chiefly splanchnic. The cutis plate extends laterally, as the embryo grows, and after thinning considerably, breaks up into a mesenchyme which spreads underneath the ectoderm, forming the foundation of the thin dermis layer of the integument.
The sclerotomal cells, multiplying and continuing the formation of intercellular substance, extend dorsally, between the nerve cord and the myotome, and ventrally, around the notochord and dorsal aorta, and finally fill all the spaces around these axial structures. Later the sclerotomes acquire a secondary segmentation, in that each becomes transversely divided opposite the middle of the somite; the posterior half of one sclerotome then unites with the anterior half of the succeeding, forming a sclerotomal segment. The sclerotome forms the axial skeleton of the embryo (except the major portion of the skull) and the segments are the rudiments of the vertebrte, which thus alternate with the muscle segments, the arrangement of which marks the primary segmentation of the embryo. All details of the formation of the skeletal system lie without the scope of the present chapter, and we shall merely call attention to the fact that the skeleton arises in part from the sclerotomes and in part from the general mesenchyme. The vertebral column is the part derived from the sclerotomes. These cells condense and the cartilaginous rudiments of the vertebra begin to appear during the fifth day around the notochord (centra) and nerve cord (neural arches). The sclerotomes of the head somites form the occipital region of the skull; the remainder of the skull is formed from the mesenchyme around the brain and sense capsules. Cartilage begins to form in the skull during the sixth day. The visceral skeleton forms from the mesenchyme of the visceral arches, cartilage appearing here during the sixth day also. The skeleton of the pectoral and pelvic arches and limbs is formed from the mesenchyme of these regions, cartilage appearing during the sixth and seventh days. The clavicles, like the derm bones of the skull and anterior visceral arches, ossify directly from mesenchyme, without being preformed in cartilage. (For simple accounts of the development of the skeleton the student is referred to Marshall, " Vertebrate Embryology/ 7 and Lillie, "Development of the Chick," where full references to the literature will be found.)
The Urinogenital System
In the chick, as in other vertebrates, the excretory and reproductive sytems arise separately and come into relation only secondarily. We may therefore begin with an account of the origin of the excretory system, and through this lead to the development of the reproductive system, and to an account of their association.
The Excretory System
The intermediate cell masses, or nephrotomes, form the rudiments of the excretory system which, as in all Amniota, is complicated by the succession of three nephric systems, pronephros, mesonephros, and metanephros, of which the first two are purely embryonic, only the last giving rise to the excretory system of the adult. The nephroi develop only through the neck and trunk regions, for in the head and tail no lateral plate, nephrotome, and somite .are differentiated in the mesodermal segment.
A. THE PKONEPHROS AND THE PRONEPHRIC DUCT (WOLFFIAN DUCT)
The pronephros is wholly of vestigial character in the chick, functionless even in the embryo. The pronephric duct, however, is retained as the duct of the embryonic kidney, and is hence known as the mesonephric or Wolffian duct. On account of its vestigial character the pronephros develops variably, even in different regions in a single individual. It is limited to the fifth to fifteenth or sixteenth somites, but becomes typically developed only in the tenth to fifteenth.
In the latter region a small bud of cells grows upward from the middle of the postero-dorsal surface of each nephrotome. These buds, appearing about the middle of the second day, are the rudiments of the pronephric tubules, so-called although they remain solid here. The buds or tubules elongate gradually, and their terminal portions bend over posteriorly, each uniting with the next posterior tubule, forming thus a continuous longitudinal strand, which is the rudiment of the pronephric or Wolffian duct. Toward the close of the second day the duct becomes hollow anteriorly. It pushes backward rapidly, above the nephrotomes, growing independently, until about the sixtieth hour it reaches the cloaca, with which it fuses; its lumen is completed throughout at the end of the third day. In front of the tenth somite no duct is formed and the tubules are reduced to small transitory buds entirely disappearing during the latter part of the second day.
Soon after the tubule appears in each segment, the nephrotome is separated from the somite by the conversion of its proximal part into mesenchyme, and the distal part then appears added to the tubule. The only cavity of the pronephric tubule is one sometimes appearing in this added portion of the nephrotome, and is to be regarded as a continuation of the ccelom of the lateral plate into the nephrotome region; when present its opening to the coelom would therefore represent a nephrostome. No Malpighian bodies are developed in connection with these tubules, and the whole pronephros disappears by the end of the third day.
B. THE MESONEPHROS
The mesonephros is the functional embryonic kidney; its duct is the original pronephric or Wolffian duct. The mesonephros begins to develop toward the end of the second day in the region immediately posterior to the pronephros. Mesonephric tubules finally develop in all segments from the thirteenth or fourteenth to the thirtieth; the most anterior tubules are thus present in segments developing pronephric tubules also. In front of the twentieth segment, however, the mesonephros remains rather vestigial and develops typically only from the twentieth to the thirtieth segments.
In this latter region the narrow nephrotomal band widens, separates entirely from the lateral plate and the somites, and the original arrangement of its cells in dorsal and ventral layers is lost. We should note that the Wolffian duct passes along, between the nephrotomes and the somatic layer of the lateral plate, while along the opposite sides of the nephrotomes is the dorsal aorta; the posterior cardinal veins soon appear just above the Wolffian ducts. On the ventral side of the nephrotome, about opposite the middle of the segment, its cells become condensed into a spherical mass, in which a definite space appears; this is the rudiment of the primary mesonephric tubule (Fig. 140). This rudiment then extends upward to the Wolffian duct with which it communicates. On the side opposite this extension another outgrowth appears which forms the Malpighian body.
Fig. 140. The development of the mesonephros. A, B. Transverse sections through the mesonephric tubules of the duck embryo with forty-five pairs of somites. After Schreiner. C. Transverse section through the middle of the mesonephros of a chick of ninety-six hours. From Lillie (Development of the Chick). Ao., Dorsal aorta; B., rudiment of Bowman's capsule; c., collecting duct; Cad., ccelom; Col. T., collecting tubule; d., dorsal outgrowth of the Wolffian duct; Glom., glomerulus; germ. Ep., germinal epithelium; M's't., mesentery; n.t., nephrogenous tissue; r., rudiment of conducting portion of primary tubule; T.I, 2, 3, primary, secondary, and tertiary mesonephric tubules; V.c.p., posterior cardinal vein; W.D., Wolffian duct.
From the nephrotome, just above the primary tubule, several additional secondary mesonephric tubules are formed, and finally, other dorsal tertiary tubules are added, so that six or seven tubules are formed in each segment; all these tubules develop similarly. No nephrostomes, or coelomic connections, are formed save in the four or five most anterior tubules, which are themselves transitory structures. The formation of the mesonephric tubules is completed during the fourth and fifth days, when they begin to elongate rapidly. During the next three or four days they become convoluted and form altogether a large mass, sometimes known as the Wolffian body, projecting from the dorsal body wall. The tubules of each segment open into a common dilation of the Wolffian duct, distinguished as the collecting tubule.
The mesonephros becomes very vascular through the formation of abundant sinuses from the accompanying posterior cardinal veins, which are its afferent vessels. The walls of these sinuses are in direct contact with the tubules. The blood collects along the ventral side of the mesonephros in the socalled subcardinal veins, which connect, as we have seen, with the inferior vena cava. The mesonephros begins to degenerate the tenth or eleventh day, and by the time of hatching it has completely disappeared, save in so far as parts of it remain connected or associated with the reproductive system.
C. THE METANEPHROS
The metanephros is the permanent kidney of the adult, and it also functions probably, together with the mesonephros, during the latter part of embryonic life. Metanephric structures appear toward the end of the fourth day as outgrowths from each mesonephric or Wolffian duct, just as this turns to enter the cloaca. Each outgrowth becomes a sac and then a tube, turning anteriorly and rapidly growing forward along the inner side of the posterior cardinal vein, and finally extending anteriorly, above the mesonephros, as far as the twenty-fifth somite. This tube is the rudiment of the ureter and collecting tubules of the metanephros; the latter are formed as the result of a complicated system of branches of the original duct as it grows forward (Fig. 141).
The secreting tubules or true metanephric tubules, are formed from the cells of the nephrotomes of the last two or three segments of the body (31-33). In this region the nephrotomal structure is not clearly differentiated, and it is referred to simply as the metanephrogenous tissue. As the metanephric diverticulum grows out it is accompanied on its inner face, throughout all its branching, by cells of this tissue. During the seventh or eighth day typical nephric vesicles appear, like those of the mesonephros, and acquire openings into each branch of the collecting duct; Malpighian bodies develop in the usual manner. During the next three or four days the entire metanephros is established, and the mesodermal cells surrounding the tubules and ducts form the stroma and capsule of the kidney. During the fifth and sixth days the terminal portions of the Wolffian ducts and the metanephric diverticula become absorbed into the wall of the cloaca so that the ureters acquire openings separate from those of the Woffian ducts; the latter are hence, after the degeneration of the mesonephros, not at all excretory in function. No nephrostomes appear in connection with the metanephros.
From the preceding description it will be seen that the inner or medullary part of the definitive kidney is derived from the branched outgrowth from the Wolffian duct, while the outer cortical layer of secretory tubules and Malpighian bodies is derived from the metanephrogenous tissue (nephrotomes) of the last two or three body somites, and is therefore homologous with the glandular part of the mesonephros.
The Reproductive System
Before describing the development of this system it seems necessary to recall, in a few words, the composition of the adult reproductive system in the Amniota. In these forms the gonoducts are derived from the original mesonephric or Wolffian duct, which is now represented by two longitudinal ducts, the Wolffian duct, stricto sensu, and the Miillerian duct. As a matter of fact, we shall see that the Miillerian duct develops independently of the mesonephric duct, but phyletically it is clear that both ducts are to be regarded as derivatives of a common mesonephric duct. The mesonephros itself largely degenerates, of course, but some part of it remains functionally connected with the reproductive system in the male, and as a purely vestigial structure in the female. Consequently in the male Amniote the Wolffian duct proper is freed from excretory function, and serves only as the gonoduct or vas deferens, effecting a connection with the gonad through the remains of certain mesonephric tubules; the Miillerian duct is either vestigial or entirely wanting. In the female, on the contrary, the Miillerian duct is the functional gonoduct, or oviduct, while the Wolffian duct and mesonephros either disappear entirely or remain as functionless vestiges.
Fig. 141. Diagram of the arrangement of the nephric elem e n t s in the chick. After Felix. Pronephric duct, and metanephric ducts (ureters) in black; meso nephric tubules cross hatched; metanephric tubules in dotted outlines.
A. THE REPRODUCTIVE DUCTS
Nothing need be added to the account already given of the development of the Wolffian duct. We shall see below how, in the male, this connects with the testis; in the female the Wolffian duct disappears along with the mesonephros.
The Miillerian ducts develop similarly in the male and female; they appear during the fourth day. Each is formed as a thickened longitudinal band in the peritoneum, along the outer surface of the mesonephros, near its attachment to the body wall, i.e., just along the outer side of the Wolffian duct. This band invaginates, forming first a groove and then a tube, lying just beneath the surface of the anterior end of the mesonephros. The extreme anterior end of this canal remains open into the body cavity, as the rudiment of the ostium or infundibulum. The greater part of the Mullerian duct is formed by the backward extension of the tube thus formed. It grows posteriorly as a solid rod, gradually becoming tubular, and reaches the cloaca during the seventh day, although it does not acquire an opening into the cloaca during embryonic life, indeed not until the fowl is about six months old. The duct becomes surrounded by a thick coat of mesenchyme cells and appears as a ridge on the surface of the mesonephros.
After the eighth day, in the male both Miillerian ducts and in the female the right duct, cease to develop and immediately begin a series of degenerative changes. In the female the left duct continues to enlarge, and as the mesonephros disappears, it remains as a conspicuous organ, attached to the dorsal body wall by a double fold of peritoneum, the mesovarium. Further differentiation into the regions of the adult oviduct already described, begins before the end of the second week of Incubation.
B. THE GONADS
The early development of the gonads is alike in both sexes, and it is not until the end of the first week that the sexes can be distinguished. This early period is known as the indifferent period. The gonads appear on the fourth day, as longitudinal bands of thickened peritoneal epithelium, along the dorsal wall of the body cavity, between the mesonephros and the attachment of the mesentery. This band of " germinal epithelium" later appears on the inner surface of the mesonephros, on account of the enlargement of this organ. The germinal epithelia develop symmetrically and extend through the posterior half or third of the mesonephric region.
The peritoneal cells of the so-called " germinal epithelium" are apparently not to be regarded as the true germ cells. As in other groups, the primordial germ cells are differentiated very early in development, and migrate into this peritoneal or germinal epithelium, where they begin to multiply (Fig. 142). The mesenchyme cells of the mesonephros, beneath the peritoneum, become added to the developing gonad and later form its stroma or connective tissues.
During the fifth day strands of cells appear, extending between the substance of the gonad and the mesonephric tubules of the region. These are the rudiments of the sexual cords (Fig. 142) . While not definitely demonstrated as yet, it seems probable that the sexual cords are outgrowths of the mesonephric tubules (Malpighian bodies) which extend into the gonad. About the end of the first week of development the sexes are distinguishable
Fig. 142. Section through the gonad of a chick, the middle of the fifth day, showing the sex cords reaching the germinal epithelium. After Semon. g, Germinal epithelium; m, epithelium of the mesentery (peritoneum); o, primitive ova; s, sex cords; t, connective- tissue stroma.
through the enlargement of the sexual cords in the male, and the greater thickness of the germinal epithelium in the female.
Testis. During the second week the primordial germ cells appear all through the stroma, and even migrate into the sexual cords, which continue to increase in size and number until they form altogether a considerable bulk. While the greater part of the mesonephros degenerates, a vestige remains as the paradidymis, that part with which the sexual cords connect. The tubules of this region become the vasa efferentia (epididymis) through the formation, about the end of the third week, of a lumen in each sexual cord, which thus puts the cavities of the testis into communication with the mesonephric tubules. The sexual cords thus become the rete e/erentia. The primordial germ cells, or spermatogonia as they may now be called, lie in the walls of the dilated inner ends of the rete efferentia (sexual cords), into the cavities of which their cell products may be discharged and pass thence, by the vasa efferentia and the vas deferens, to the cloaca. The original "germinal epithelium" becomes converted into a flat covering layer continuous with the peritoneal folds (mesorchia) slinging the testis from the dorsal body wall.
Ovary. The early development of the ovary parallels that of the testis. Like the right oviduct, the right ovary, after developing for a time, degenerates and disappears. In the left or definitive ovary the primordial germ cells behave as in the testis, at first, but after a brief period their migration ceases and those which have left the primitive germinal epithelium degenerate, together with the sexual cords. The epithelial cells, and the primordial germ cells contained in the epithelium, continue to multiply rapidly, and the mesenchymal stroma becomes abundant. The inner surface of the germinal epithelium forms strands of cells projecting into the stroma of the ovary, and containing primordial germ cells or oogonia. These strands segment into separate cell masses or nests, each including an oogonial cell; the further growth and development of the oogonia have been described in the beginning of the preceding chapter.
The mesonephros thus has no share in the formation of the reproductive system of the female; its posterior section may be recognized in the vestigial paroophoron, while the homolog of the epididymis of the male is to be seen in the parovarium.
C. THE ADRENAL BODIES
Brief reference to the development of the adrenal bodies may be made here, although they are not a part of the renal system. These bodies have a double origin, arising in part from peritoneal proliferation and in part from sympathetic ganglion cells; the part derived from the peritoneal cells effects secondary connections with certain mesonephric components.
During the fourth day the peritoneal cells in front of the germinal epithelia proliferate and extend through the mesenchyme anterior to the mesonephroi and along the dorsal aorta. As these cells multiply they become arranged in definite strands or solid cords; these cords then connect with the renal vesicles of the adjacent portion of the mesonephros. By the eighth day a definite and highly vascular rudiment is established on each side. About this time cells of a sympathetic ganglion located on the antero-dorsal side of the adrenal rudiment, begin to extend into it, penetrating among the primary cords. During the later stages these peritoneal and sympathetic components assume the relations found in the adult adrenal, forming then the cortical and medullary cords respectively.
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|Outlines of Chordate Development 1913: 1. Amphioxus | 2. Early Frog | 3. Later Frog Organogeny | 4. Early Chick - Embryonic Membranes and Appendages | 5. Later Chick - Organogeny | 6. Early Mammal - Embryonic Membranes and Appendages | Figures|
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