Book - The development of the chick (1919) 6

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Lillie FR. The development of the chick. (1919) Henry Holt And Company New York, New York.

Lillie 1919: Introduction | Part 1 - 1 The Egg | 2 Development Prior to Laying | 3 Outline of development, orientation, chronology | 4 From Laying to Formation of first somite | 5 Head-fold to twelve somites | 6 From twelve to thirty-six somites | Part 2 - 7 External form of embryo and embryonic membranes | 8 Nervous system | 9 Organs of special sense | 10 Alimentary tract and appendages | 11 The body-cavities, mesenteries and septum transversum | 12 Later development of the vascular system | 13 Urinogenital system | 14 Skeleton | Appendix | Frank Lillie

Part I The Early Development to the End of the Third Day

Chapter VI From Twelve to Thirty-Six Somites

Thirty four To Seventy-Two Hours

I. Development of the External Form, and Turning of the Embryo

In the embryo of twelve somites only the head is distinctly separated from the blastoderm; and there is no sharp boundary between the embryonic and extra-embryonic portions of the blastoderm in the region of the trunk; but this changes very rapidly. The progress of the developmental processes, that have marked out an embr^^onic axis in the blastoderm, produces in the course of about eighteen hours a sharp distinction everywhere between embryo and extra-embryonic blastoderm. The latter, together with an outgrowth of the embryonic hind-gut (allantois), then constitute the so-called embryonic membranes, which become very complicated, and which provide for the protection, respiration, and nutrition of the embrvo. We shall consider the formation of the embryonic membranes separately in order not to confuse the account of the development of the external form of the embrvo.

In considering the development of the external form of the embryo, we must distinguish between those processes that separate it from the extra-embryonic blastoderm, and those that occur within its own substance leading to various characteristic bendings and flexures; we may consider them separately, although they are going on at the same time.

Separation of the Embryo from the Blastoderm. The separation of the embryo from the blastoderm takes place by the formation of certain folds or sulci that may be named: (1) the head-fold or anterior limiting sulcus; (2) the lateral limiting sulci, appearing as prolongations of the head-fold along the sides of the embryonic axis; and (3) the tail-fold or posterior limiting sulcus.

The head-fold has been described in detail in the preceding chapter. The lateral limiting sulci are a continuation of the lateral limbs of the head-fold; they owe their origin to the folding of the splanchnopleure and somatopleure adjacent to the embryo towards the yolk, at the line of junction of embryonic and extraembryonic parts. The tail-fold arises about the stage of 26 to 27 somites (Fig. 93), and is similar to the head-fold, except that it is turned in the opposite direction. The sulci combine to form a continuous ring around the embryo and gradually pinch it off, so to speak, from the extra-embryonic blastoderm.

In the splanchnopleure the lateral limiting sulci (Fig. 69) come together and fuse both in a caudal direction from the foregut, and subsequently in a cephalic direction from the hind-gut (see below), so as to convert the splanchnic gutter into a tube (the alimentary canal). There is thus a ventral suture along the alimentary canal in which the entoderm of the alimentary canal becomes separated from the extra-embryonic entoderm, leaving a double layer of the splanchnic mesoblast (ventral mesentery) connecting the alimentary canal with the extra-embryonic splanchnopleure; but this disappears everywhere as soon as formed, except in the region of the posterior part of the heart and the liver, where it forms the dorsal mesocardium and gastro-hepatic ligament (Fig. 118), and in the region of the neck of the allantois.

Fig. 69. - Transverse section through the fifth somite of the 23 s stage.

Amnion. Ao., Aorta, a. i. p., Anterior intestinal portal. Coel.,

Ectamnion. E. E. B. C, Extra-cmhry1. 1. s., Lateral limiting sulcus. My.,

Amn Coelome. Chor., Chorion. Ectam., onic body-cavity. Int., Intestine.

Myotome, s. a., Segmental artery. So'pl., Somatopleure. Spl'pl., vSplanch noplcure. s., Somite, s. 5, Fifth somite. V. O. M. R. and L., Right and left omphalo-mesenteric veins. V. V., Vitelline vein.

The fore-gut is thus being continually lengthened backwards by fusion of the lateral limbs of the splanchnopleure. At the 31 s stage this has proceeded about to the fourteenth somite. At about the 21 s stage the tail-fold appears in the splanchnopleure, thus establishing the hind-gut (Fig. 70) which gradually elongates forwards. There remains then an open portion of the alimentary tract, where its walls are continuous with the extraembryonic splanchnopleure or yolk-sac. This is known as the yolk-stalk. The entrance from the yolk-sac into the fore-gut is known as the anterior intestinal portal, and that from the yolk-sac into the hind-gut as the posterior intestinal portal (Fig. 70). At the 27 s stage the yolk-stalk is long and narrow (Fig. 106); the stems of the splanchnic (omphalo-mesenteric) veins run to the heart in its anterior portion, and the omphalo-mesenteric arteries pass out about its center. As it gradually closes, the stems of the omphalo-mesenteric arteries and veins are brought closer together. At about five daj's it becomes a tubular, thickwalled stalk, connecting intestine and yolk-sac, and so remains throughout embryonic life.

Fig. 70. — Median longitudinal section through the hind end of an embryo of about 21 s. an. pi., Anal plate, an. t., Anal tube. p. i. p., Posterior intestinal portal. T. B., Tail-bud. t. f. So'pL, Tail fold in the Somatopleure. t. f. Sp'pl., Tail fold in the splanchnopleure. Other abbreviations as before.

The limiting sulci in the somatopleure lead to the formation of the body-wall. In the trunk the somatopleure is separated from the splanchnopleure by the coelome (Fig. 69), and the folds in the somatopleure take the same general direction as those in the splanchnopleure; they thus lead to the formation of a tube (body-wall) outside of a tube (alimentary canal), the intervening cavity being the body-cavity. The unclosed part of the bodywall is continuous with the extra-embryonic somatopleure, more specifically the amnion (see below), and this connection is known as the somatic stalk or umbilicus. The yolk-stalk and neck of the allantois pass out of the body-cavity through the somatic stalk, which therefore remains open until near the end of incubation.

The Turning of the Embryo and the Embryonic Flexures. We have described the separation of the embryo from the extraembryonic blastoderm without reference to its turning from a prone to a lateral position or to the formation of the flexures of the entire head and body that are so characteristic of amniote embryos generally. These changes begin about the 14 s stage and are first indicated by a slight transverse bending of the originally straight axis of the head in the region of the mid-brain (Fig. 67). By means of this bending, known as the cranial flexure, the fore-brain is directed toward the yolk; but almost simultaneously another tendency manifests itself, viz., rotation of the head on its side, at first affecting only the extreme end. (See Figs. 71, 73, 99, etc.) By the 27 s stage these two processes have resulted in the conditions shown in Fig. 105: by the cranial flexure the fore-brain is bent at right angles to the axis of the embryo, and owing to the rotation the head of the eml^ryo lies on its left side. But inasmuch as the trunk is still prone on the surface of the volk the axis of the embrvo is twisted in the intermediate region. This twist is transferred farther and farther backwards as the turning of the head gradually involves the trunk, until finally, at about ninety-six hours, the embryo lies entirely on its left side.

Exceptionally the rotation may be in the inverse direction (heterotaxia) ; in such cases it is often associated with situs inversus viscerum. Heterotaxia has been produced experimentally (Fol and Warynsky).

After the appearance of the cranial flexure a second transverse flexure appears in the embryo, this time at about the junction of head and trunk, hence known as the cervical flexure (Figs. 73, 99, etc.). This flexure gradually increases in extent until the head forms a right, or even smaller, angle with the trunk; thus the fore-brain is turned to such an extent that its anterior end points backwards and its ventral surface is opposed to the ventral surface of the throat (Fig. 117).

Fig. 71. — Entire embryo of 16 s, drawn from above as a transparent object. Note the cranial flexure; the rotation of the head on its left side is beginning, au. P., Auditory pit. F. B., Fore-brain. H. B. 1, First division of the hind brain. H. F. Am., Head-fold of the amnion. Hm. F., Hyomandibular furrow. Pr'am., Proamnion. M. B., Mid-brain, op. Yes., Optic vesicle, pr. str., Primitive streak, s 2, s 4, s 16, Second, fourth, and sixteenth somites. V. o. m., omphalo-mesenteric vein. ^TI-V^I, The acustico-facialis primordium. IX-X, Primordium of the glossopharyngeus and vagus.

The entire trunk tends also to bend ventrally, i.e., to develop a dorsal convexity, and this approximates its posterior end to the tip of the head. These flexures are characteristic of amniote vertebrate embryos; the cause appears to lie in the precocious development of the central nervous system, of which more hereafter. Only the cranial flexure remains as a permanent condition.

II. Origin of the Embryonic Membranes

The period from about 12 to 36 somites also includes the early history of the embr3^onic membranes, amnion, chorion, yolk-sac and allantois. The first three arise from the extra-embryonic blastoderm, and the allantois arises as an outgrowth of the ventral wall of the hind-gut.

Fig. 72. — The head of the same embryo from below.

a. i. p., Anterior intestinal portal. B. a., Bulbils arteriosus. Inf., Infundibuliim. or. pi., Oral plate. Tr. a., Truncus arteriosus. Ven., Ventricle, v. Ao., Ventral aorta.

Origin of the Amnion and Chorion

The amnion is a thin membranous sac, forming a complete investment for the embryo and continuous with the body-wall at the umbilicus; it lies beneath the chorion to which it remains attached throughout incubation by a plate of tissue (sero-amniotic connection), and it arises in common with the chorion from the extra-embryonic somatopleure. The entire somatopleure external to the embryo is used up in the formation of these two membranes. The amnion arises from a portion immediately adjoining the embryo itself; the remainder of the somatopleure peripheral to the amniogenous part forms the chorion. Thus the extra-embryonic somatopleure may be divided into two zones; an amniogenous zone immediately adjacent to and surrounding the embryo, and a choriogenous zone, comprising the remainder.

Fig. 73. — Entire embryo of 20 s, viewed as a transparent object from above. The cranial flexure and the rotation of the head of the embryo have made considerable progress. A. o. m., Omphalo-mesenteric artery. Or. Fl., Cranial flexure. D. C, Duct of Cuvier. Dienc, Diencephalon. Mesenc, Mesencephalon. Metenc, Metencephalon. Myelenc. 1, and 2, Anterior and posterior divisions of the myelcncephalon. Telenc, Telencephalon. Vel. tr., Velum transversum. Other abbreviations as before, x 30.

The method of formation of amnion and chorion is as follows:

(a diagrammatic outline is first given and a detailed description follows). The somatopleure becomes elevated in the form of a fold surrounding the embryo; this fold begins first in front of the head of the embryo as the head-fold of the amnion which immediately turns backwards over the head, forming a complete cap (Figs. 67, 71, 75, etc.); the side limbs of the head-fold are then elongated backwards, and are here known as the lateral folds of the amnion; these rise up and arch over the embryo (Figs. 109 and 110). In each fold one can distinguish an amniotic or internal limb, and a chorionic or external limb meeting at or near the angle of the folds, the line of junction being marked by an ectodermal thickening, the ectamnion. Fusion of the right and left lateral folds begins at the head-fold, and progresses backwards in such a way that the right and left amniotic limbs become continuous with one another, similarly the right and left chorionic limbs; and, when fusion is complete, the amnion and chorion become separate continuous membranes. In this way the amnion extends, by the 27 s stage, back to the seventeenth somite (Fig. 105). At this time a new fold arises behind the rudimentary tail-bud and covers the tail precisely as the headfold covers the head (Fig. 105) ; the tail-fold of the amnion then apparently is prolonged forward a short distance and soon meets the anterior lateral folds, forming a continuous lateral fold. Fusion continues until, about the 31 s stage, the opening into the amniotic cavity is reduced to a small elliptical aperture lying above the buds of the hind-limbs (Fig. 99). This then rapidly closes, but a connection, sero-amniotic connection, remains at the place of final closure. Elsew^here the separation of chorion and amnion is complete.

Fig. 74. — Head of the same embryo from the ventral side. Abbreviations as before.

Fig. 75. — Median sagittal section of the head of an embryo of 18 s.

H. F. Am., Head-fold of the amnion. Ph., Pharynx. Isth., Region of the isthmus, pr'o. g., Preoral gut. or. pi., Oral plate. Ree. opt., Recessus opticus. S. v., Sinus venosus. Other abbreviations as before.

The formation of the amnion is an extremely interesting process from the standpoint of developmental mechanics, and involves a number of details that are best understood after such a general review of the process as has been given in the preceding paragraphs. Returning then to the 12 s stage for consideration of these details, we must first note that the extension of the mesoblast prior to this period has left an area situated in front of the head free from mesoblast (Figs. 65, 67, 71, 75, etc.). This area, in which the ectoderm and entoderm are in contact, is known as the proamnion. The formation of the amnion begins within this area by a thickening in the ectoderm (ectamnion) near the anterior boundary of the proamnion at a stage with about eight or nine somites. The thickening, which is very narrow, extends right and left, and turns backwards along the sides of the head to about the region of the middle of the heart, gradually becoming more peripheral in position and fading out (Fig. 76). It represents the junction of the amniogenous and choriogenous somatopleure and thus corresponds to the angle of the future amniotic folds. The head of the embryo lies in a depression bounded in front by the ectamnion, and on the sides by the amnio-cardiac vesicles of the body-cavity (Fig. 65). The floor of the depression is the proamnion. Just before the formation of the head-fold proper, the ectamnion in front of the head becomes irregularly thickened to such an extent as sometimes to present an actually villous surface (Fig. 77; cf. Fig. 67).

The head-fold of the amnion begins to form at about the same time as the cephalic flexure. The great expansion of the body-cavity on each side of the head (amnio-cardiac vesicles) causes an elevation of the anterior angle of the ectamnion, and a pocket is formed by fusion of its lateral limbs. This slips over the head of the embryo with aid of the ventral flexure of the head just developing. Inasmuch as the anterior angle of the ectamnion is in the proamnion, where there is no mesoderm, and where the ectoderm is in immediate contact with the entoderm, the entoderm as well as the ectoderm of the proamnion is drawn into the head-fold, so that the latter is not at first a fold of the somatopleure. But in the chick the proamniotic part of the head-fold is

, 1 , , A. Region of the soma never very extensive and does not at any topleure destined to form

time extend back of the beginning of the body-wall.

^1 .... ,, . . . B. Amniosrenous soma the mid-bram. Moreover, it is soon in- topleure.

vaded (Fig. 75) bv the bodv-cavitv, and ^- Choriogenous soma then the entoderm is withdrawn and becomes part of the general splanchnopleure. The proamnion ventral to the head is not invaded by mesoderm until a much later period.

The ectodermal thickening marking the junction of amniotic and chorionic somatopleure extends backwards very rapidly and always precedes the origin of folds in any region. The lateral folds themselves appear to owe their origin to the progressive fusion of the ectodermal thickenings of the opposite sides, beginning at the posterior angle of the head-fold and proceeding backwards. The energy of fusion is sufficient in itself to lift the somatopleure up in the form of a fold around the body of the embryo. Thus new parts of the ectodermal thickening are constantly being brought together and the fusion progresses steadily, and this in its turn prolongs the lateral amniotic folds. These possess no independent power of elevation of any considerable amount, for, when the initial fold of one side is destroyed by cauterization, the fold of the opposite side remains as an insignificant elevation in the somatopleure a long distance lateral to the embryo.

Fig. 76. — Entire embryo of 13 s, to shoAV the relations of the ectamnion. a. c, Inner margin of amnio-cardiac vesicles, e. a., Ectamnion.

Fig. 77. ■ — Transverse section through the anterior angle of the eetamnion a few sections in front of the tip of the head.

Stage of 14-15 s. b. c Extra-embryonic body-cavity, c, Cavity in the entoderm, e. a., Eetamnion.

The tail-fold arises in an analogous manner to the head-fold, except that there is no proamnion here. The progress of the various folds and their final fusion follows from what has already been said.

Practically all of the somatopleure of the pellucid area is amniogenous with the exception, naturally, of that part internal to the limiting sulci that forms the body-wall. What effect has the turning of the embryo on its left side on the amniogenous somatopleure? We will suppose that the latter is primitivelv of equal width on both sides and that the notochord represents approximately the axis of rotation. During the process of rotation, the embr3'0 sinks and the lateral limiting sulci become deeper. A direct consequence of the rotation must be, therefore, a strong tension on the somatopleure belonging to the under (left) side, a-h, and practically none on the upper (right) side, c-d. (See Fig. 78 A, B).

Even though the difference may be partly compensated by drawing of the embryo to the left, the tendency would be to stretch a-h. If there were no such compensation and a and b were practically fixed points, the length of a-b at the conclusion of the rotation would much exceed that of c-d (Fig. 78 B), and if, during this process, there were actual independent growth of a-b and c-d, the latter would of necessity be thrown into folds, but not the former. Finally, if the amniotic folds were forming at the same time (as is actually the case), the right one would inevitably be thrown into secondary folds by the approximation of points c and d (Fig. 78 C).

Fig 78. A, 5, and C. Diagrams to represent the effect of rotation of the embryo on the amniogenous somatopleure. a represents in all figures the position of the ectamnion on the left (lower) side; d represents in all figures the position of the ectamnion on the right (upper) side, h and c represent the junction of amnion and body-wall on left and right sides respectively. In Fig. A, a-b and c-d are equal. In Fig. B, rotation of the embryo is assumed to have taken place without formation of the amnion; the distance a-b has become greater than c-d. In Fig. C is represented rotation of the embryo with synchronous formation of the amniotic folds, as is actually the case; c-d is inevitably thrown into secondary folds. The vertical lines at the extreme right and left represent the margins of the pellucid area.

Study of the fusion of the amniotic folds in actual sections shows, that the line of fusion of the opposite amniotic limbs is over the dorsal surface of the embryo only so long as the latter lies flat on the yolk; it does not follow the turning of the embryo on to its left side, and the consequence is that, after rotation of the embryo, the line of fusion lies over the upper (right) side of the embryo, often opposite the horizontal level of the intestine (Fig. 79). Thus one fold of the amnion passes all the way from the under side over the back of the embryo and around on the other side to the line of fusion, and thus is several times as long as the opposite limb. Moreover, the amniotic fold of the right side is invariably thicker than that of the left side, and is always thrown into secondary folds at the place of turning (Fig. 79). These conditions are satisfactorily explained, as noted above, by the mere turning of the embryo on its side.

Fig. 79. — Section of an embryo of about 60 hours to show the secondary fold (s. f .) of the amnion on the right side. e. a., Ectamnion. s. f., Secondary fold. 1., Left. r. Right.

One must therefore distinguish in the upper limb of the amnion two kinds of folds: (1) The ordinary amniotic fold induced by the fusion of the right and left folds, and (2) secondary folds formed simply by the process of twisting of the embryo.

These secondary folds of the amnion are very transitory, except in two regions: (1) Above the hind end of the heart (apex of ventricle), and continuing a short distance behind it; (2) in the region immediately in front of the allantois, at sixty to seventy hours, thus in the neighborhood of the final closure of the amniotic folds. The former are of very constant occurrence and persist a long time (Fig. 93).

Elsewhere the effect of the twisting of the embryo is rapidly compensated so that the secondary folds of the right half of the amnion do not persist long.

The subsequent history of the amnion and chorion is given in another place. It should be noted here that the chorion, at the stage of seventy-two hours, is continuous peripherally with the splanchnopleure at the margin of the vascular area, and that it ])ecomes separate from it only as the body-cavity extends more and more peripherally. The sero-amniotic connection remains throughout the entire embryonic period and modifies in an important fashion the subsequent history of the membranes.

The yolk-sac is the name given to the extra-embryonic splanchnopleure, because in the course of expansion of the blastoderm and extension of the extra-embryonic body-cavity over the surface of the yolk, it finally becomes a separate sac enclosing the yolk. It remains connected by the yolk-stalk with the intestine until finally, some time after hatching, it is absorbed completely. The yolk is absorbed by the entodermal lining and is carried to the embryo in solution by means of the vitelline veins.

Origin of the AUantois

The allantois arises as a diverticulum of the hind-gut soon after the formation of the latter by the tailfold. It is not indicated before the formation of the tail-fold as stated by some authors, but the tube identified by them as the primordium of the allantois at this early stage is really the intestinal diverticulum leading to the anal plate (Fig. 70). At the stage of twenty-eight somites the allantois is indicated by the depth of the hind-gut, the ventral portion of which in front of the anal plate soon becomes constricted from the upper portion, and forms the primordium of the allantois. In longitudinal sections of an embryo of about thirty-five somites it can be seen to include nearly the entire floor of the hind-gut between the anal plate and the posterior intestinal portal (Fig. 80). It is lined with entoderm and has a thick mesodermal floor in which numerous small blood-vessels are already present. A transverse section (Fig. 81) shows that the thick mesodermal wall is broadly fused with the somatopleure in the region of the neck. In other words, the allantois is developed within the ventral mesentery. It will also be seen by comparing these figures that the amnion arises from the neck of the allantois both behind and also at the sides, (cf. Fig. 82.)

During the fourth day the distal portion of the allantois pushes out into the portion of the extra-embryonic body-cavity beneath the hind end of the embryo and rapidly expands to form a relatively large sac. But the neck of the allantois remains embedded in the ventral mesentery and does not expand; the terminal portion of the intestine has in the meantime formed the primordium of the cloaca, from which, therefore, the neck of the allantois appears to arise (Fig. 183) ; at all stages of incubation the neck of the allantois forms an open connection between the cloaca and the allantoic sac.

Fig. 80. — Sagittal section through the tail of an embryo of about 35 s.

All., Allantois. An. pi., Anal plate, c. C, Central canal of the neural tube. CL, Cloaca. Ectam., Ectoderm of the amnion. Mesam., Mesoderm of the amnion, p'a. G., Post-anal gut. p. i. p., Posterior intestinal portal. s. A., Segmental arteries. Other abbreviations as before.

The Umbilicus. The closure of the body-wall progressively reduces the communication between the embryonic and extra-embryonic body-cavity to a narrow chink between the yolk-stalk and allantoic stalk on the one hand and the attachment of the amnion on the other. The mnbilical cord thus consists of an outer tube (somatic stalk) continuous with the body-wall, enclosing the yolk-stalk and the stalk of the allantois, together with the arteries and veins of yolk-sac and allantois. It is important to bear in mind that in the region of the neck of the allantois the amnion is attached to the latter at the sides and behind; only the anterior wall of the allantoic stalk is free (Fig. 82). In other words, the somatic umbilical stalk is fused with the lateral and caudal wall of the neck of the allantois, a relation that is common to all amniota.

Fig. 81. — Transverse section through the hind-gut and allantois of an embryo of 35 s; the section passes through the thirtieth somite. Details diagrammatic. All, Allantois. H. G., Hind-gut. L. B., Leg bud. v. M., Ventral mesentery. W. I)., Wolffian duct. Other abbreviations as before.

Summary of Later History of the Embryonic Membranes

The full history of the embryonic membranes will be given later (Chap. VII), but it seems desirable to give an outline here in order to avoid repeated recurrence to this subject. The extension of the body-cavity in the blastoderm is at first very rapid, but about the fifth day it becomes slow, and the yolk-sac is never completely separated from the chorion. The allantois extends out into the extra-embryonic body-cavity as a small pear-shaped vesicle by the end of the fourth day. It then enlarges very rapidly and extends in the form of a flattened sac over and around the embryo immediately beneath the chorion with which it forms an inseparable union. As the extra-embryonic body-cavity extends, the allantois continues its expansion between the chorion and the yolk-sac, and finally wraps itself together with a duplication of the chorion, completely around the albumen of the egg, which has become very viscid, and aggregated in a lump opposite to the embryo. The allantois is very vascular from the start, and serves as an embryonic organ of respiration. It also receives the excretion of the embrvonic kidneys and absorbs the albumen.

Fig. 82. — Model of the caudal end of a four-day chick to show the relations of the amnion to the allantois and umbilicus. (After Ravn.)

All., Neck of the Allantois. Am., cut surface of the amnion. A. o. m., Omphalo-mesenteric artery. an. pi., Anal plate. L. B., cut surface of leg bud. T., Tail.

The yolk-sac becomes much shriveled during incubation owing to absorption of its contents, and on the last day of incubation is withdrawn into the body-cavity through the umbilicus, which finally closes. The chorion, amnion, and allantois shrivel up when the chick begins to breathe air, and are cast off with the shell at hatching.

III. The Nervous System

The Brain

The description of the nervous system in the preceding chapter forms our starting-point. During the period now under consideration the foundation of the main parts of the adult brain are laid down, and its five chief divisions become sharply characterized. It is important to correlate these with the earliest morphological characters (original anterior end of medullary plate, neuromeres, etc.) in order to trace these fundamental landmarks through to definitive structures.

As we have already seen, the primary fore-brain includes the first three neuromeres, the mid-brain the fourth and fifth, and the hind-brain the sixth to the eleventh, as well as the region opposite to the first four mesoblastic somites. It is clear that a second point of fundamental morphological significance is the original anterior end of the medullary plate which would naturally form the center for a description of the anterior part of the neural axis, if recognizable throughout the development. This point may be recognized for a considerable period after the closure of the anterior part of the neural tube, as the ventral end of the -anterior cerebral fissure (Fig. 62), opposite the center of the primary optic vesicles, thus in the region of the recessus opticus (Figs. 87 and 88), which is to be regarded as marking the original anterior end of the neural axis. Even after closure of the anterior cerebral fissure a connection remains at its dorsal end between the ectoderm and the neural tube. To this we may apply the name neuropore, though no actual opening is found here at this time. The median stretch of tissue between the recessus opticus and the neuropore constitutes the lamina terminalis which remains as the permanent anterior wall of the neural tube. It must not be forgotten that the original anterior end of the medullary plate lies at the ventral end of the lamina terminalis, i.e., in the recessus opticus. A third landmark of fundamental morphogenic significance is the infundibulum, which coincides in position, as we have seen, with the anterior end of the notochord. Thus we may distinguish prechordal and suprachordal portions of the neural axis (cf. Fig. 67).

Dorsal and Ventral Zones in the Wall of the Brain

The conception of His, that the walls of the neural tube may be considered as formed of four longitudinal strips, viz., floor, roof, and two lateral walls, is a useful one. Each lateral wall may also be divided into a dorsal and ventral zone, the former of which is related to the sensory nerve roots and the latter to the motor.

Fig. 83. — Five stages in the history of the neuromeres of the brain of the chick. (After Hill.) All figures drawn from preparations of the embryonic brain dissected out of the embryo.

A. Neural groove in an embryo with 4 somites. Right profile view, x 44.

B. Brain of a 7 s embryo, 26 hours old. Dorsal view; the three anterior neuromeres are practically obhterated. x 44.

C. Brain of 14 s embryo. Dorsal view, x 44. The neuromeres have now disappeared in the mid-brain rearion.

D. Right side of the brain of a chick embryo. 47 hours old. x 44.

E. Right side of the brain of an embryo, 80 hours old. x 17.

1-11, Neuromeres 1 to 11. IH, V, VII, interneuromeric grooves. A'f., Root of acustico-facialis (seventh and eighth cranial nerves), au. vs.. Auditory pit. ep., Epiphysis, r., Groove between the tel- and diencephalon. s., Groove between the par- and synencephalon. Tr., Root of trigeminus.

Cerebral Flexures

The cerebral flexures correspond to the cranial and cervical flexures of the entire head already described. Their form and rate of progress may be more readily learned from the figures (Figs. 67, 73, 83, etc.) than from any verbal description. Only the cranial flexure is permanent, and the angle thus formed ventrally in the floor of the mid-brain is known as the plica encephali ventralis. A third flexure is formed later in the anterior portion of the hind-brain, by a ventral bending of the floor which is barely indicated in the period now under description, but becomes much more pronounced later; this is known as the pontine flexure.

We may now take up separately the changes in each of the primary cerebral vesicles.

The Prosencephalon

The principal events in the early development of the prosencephalon are: (a) the separation of the optic vesicles; (h) the delimitation of the tel- and diencephalon; (c) special differentiation of the walls.

(a) A section across the optic vesicles of the 12 s chick shows the prosencephalon as a central division with its cavity widely confluent with the cavities of the optic vesicles. This wide communication is rapidly narrowed by a ventrally directed fold of the roof at the line of junction of the optic vesicles and prosencephalon proper (Fig. 84); the fold also involves to a certain extent the anterior and posterior line of junction. In the 20 s embryo the connection of the optic vesicles and prosencephalon has been reduced in this way to about one third of its original diameter (from actual measurements), forming a narrow tubular stalk, the optic stalk, attached to the ventral portion of the fore-brain (Figs. 73 and 74); the cavities of the optic vesicles are still continuous through the stalk with the cavity of the prosencephalon, dipping into the recessus opticus; the ventral wall of the optic stalk thus becomes continuous with the floor, and the dorsal wall with the lateral wall of the prosencephalon (Fig. 84). Growth of the mesenchyme situated above the original optic stalk appears to be an active factor in the separation; at least it grows at a rate sufficient to fill in the space produced by the constriction. At the same time there is a slight increase in the dorso-ventral diameter of the fore-brain itself, though this is relatively slight up to twenty somites, but it enhances the general effect of the change in position of the optic stalk. The subsequent history of the optic vesicles is given beyond.

(b) The delimitation of the tel- and diencephalon is initiated by a forward expansion of the anterior end of the primary forebrain, which becomes the telencephalon or secondary fore-brain, the remainder being then known as the diencephalon or 'tween brain. The expansion proceeds very rapidly from the 14 s stage, and it is probable that it involves only the dorsal zones. It is, however, difficult to establish an exact line of demarcation between the two subdivisions of the primary fore-brain, until about the 18 to 20 s stage, when a slight transverse fold or indentation in the roof (velum trans versum) gives a dorsal landmark (Figs. 73, 85); the recessus opticus forms the ventral boundary between the two. The velum transversum lies a considerable distance above the dorsal end of the lamina terminalis, but it is difficult to say just how far, owing to the indefiniteness of this point for some time after the disappearance of the neuropore. A line drawn between the velum transversum and the recessus opticus mav be taken as the boundary between the two divisions of the primary fore-brain; but, owing to the simultaneous lateral expansion of the telencephalon, the line of separation in the lateral walls forms a curve with the convexity directed posteriorly (Figs. 83 E and 86).

Fig. 84. — Transverse section through the fore-brain and optic vesicles of a 16-s embryo. Am. F., Amniotic fold. Ectam., Ectamnion. L., Left side,, Optic stalk. R., Right side. Other abbreviations as before.

(c) The next stage in the differentiation of the telencephalon (20 s to 36 s) is characterized by a rapid expansion and evagination of its lateral walls, while the entire median strip extending from the velum transversum to the recessus opticus remains practically unaltered, and thus acts like a rigid band stretched over the surface between these two points. The effect of this is to form a pair of outgrowths that soon begin to project dorsally, anteriorly, and posteriorly (Fig. 83 E); these are the primordia of the cerebral hemisi:)heres, the cavities of which thus appear as lateral diverticula of the median cavity of the telencephalon (Fig. 86). The central part of the telencephalon may be called the telencephalon medium, and the lateral outgrowths the hemispheres. The walls of the hemispheres become considerably thicker in this period, but quite uniformly at first, so that the distinction between mantle and basal ganglia is indicated only by position. (See Chap. VIII.)

FiG. 85. — Optical sagittal section of the head of an embryo of 22-23 s. The heart is represented entire. Atr., atrium. Hyp., anterior lobe of the Hypophysis. Inf., Infundibulum. Md., Mandibular arch, or.' pi., Oral plate. Pr'o. G., Preoral gut. Th., First indication of thyroid. T. p., Tuberculum posterius. V. tr., Velum transversum. Other abbreviations as before.

The median strip includes the tela choroidea, beginning at the diencephalon, and the lamina terminalis, which ends at the recessus opticus. These divisions are of great prospective significance, though at the stage of 36 s they are but slightly differentiated, save by their position. A slight thickening of the lamina terminalis just in front of the recessus opticus marks the site of the future anterior commissure (Figs. 87 and 88).

Fig. 86. — Inner view of the brain of a chick of al^oiit 82 hours, drawn from a dissection. Ch. opt., Chiasma opticus. Ep., Epiphysis (pineal gland). Isth., Isthmus. Pl.enc. v., PHca encephah ventrahs. Rec. opt., Recessus opticus. V. tr., Velum Transversum. Other abbreviations as before.

The Diencephalon

The portion of the primary fore-brain posterior to the telencephalon is known as the diencephalon. It includes the second and third neuromeres and probably also the ventral zones and floor of the first (Fig. 83). A slight constriction in the roof that appears about the 18 to 20 s stage near the junction of the middle and last third may represent the boundary between the second and third neuromeres; this persists for a long time and may be traced in the lateral walls to the region of the infimdibiilum (Fig. 83 E) ; thus the diencephalon may be divided into an anterior and posterior division, parencephalon and synencephalon (Kupffer) (Fig. 87). Tlie optic stalks are attached to the floor and ventral zones at the extreme anterior end. The diencephalon includes part of the roof, floor, and dorsal and ventral lateral zones of the original neural tube. These may be described as follows (Figs. 87 and 88):

Fig. 87. — Optical longitudinal section of the head of an eml^ryo of 30 s. The heart is represented entire. Atr., Atrium (auricles). B. a., Bulbus arteriosus. D. v., Ductus venosus. Lg., Laryngo-tracheal groove. Oes., Oesophagus, or. pi., Oral plate, which has begun to rupture. Parenc, Parencephalon. Ph., Pharynx. Stom., Stomach. Synenc, Synencephalon. Th., Thyroid. S. v., Sinus venosus. Yen. R., Right ventricle. Other abbreviations as before.

The roof rises quite sharply from the velum transversum, and is indented between the parencephalic and synencephalic divisions as already noticed. It is relatively thin. About the 3035 s stage the epiphysis (pineal body) begins to form as an evagination from about the middle, and by the 36 s stage is a small hemispherical protuberance (Figs. 86 and 88). The floor becomes extremely thin in the center of the recessus opticus, which marks its anterior end; immediatelv behind this is a sudden and conspicuous thickening, the optic chiasma, which is continued as a ridge in tlie lateral ventral zones on each side (Fig. 86). The infunclibulum follows just behind this, and constitutes a considerable pouch-shaped depression from which the saccus infundibuli grows out later. The posterior wall of this depression rises sharply and joins the thickened tuberculum posterius which is the end of the floor of the diencephalon. The diencephalon is compressed laterally (Fig. 97); the dorsal zones are slightly thickened, indicating the future thalami optici.

Fig. 88. — Optical longitudinal section of the head of an enil^ryo of 39 s. Abbreviations as before.

The anterior lobe of the hypophysis should be mentioned here, although it is not embryologically a part of the brain. It arises as a median tubular invagination of the ectoderm of the ventral surface of the head immediately in front of the oral plate at about the 20 s stage (Fig. 85), and grows rapidly inward in contact with the floor of the diencephalon. At about the 30 s stage its end reaches nearly to the infimdibulum (Fig. 87). At first part of its wall is formed by the oral plate, and when this ruptures the effect is to shorten the apparent length of the hypophysis (Fig. 88) . At about the 36 s stage its distal portion flattens laterally and shows indication of branching. Subsequently it becomes much branched and quite massive and unites with the infundibuhim to form the pituitary body. (See Chap. VIII.)

The Mesencephalon

This portion of the brain comes to occupy the summit of the cranial flexure, which indeed owes its origin largely to the rapid growth in extent of the roof of the mesencephalon. In longitudinal section it thus appears wedgeshaped, with short floor and long arched roof (Figs. 87 and 88). Its walls remain of practically uniform thickness up to the seventy-second hour. The lateral walls expand more rapidly than the roof and thus form the optic lobes. But these are barely indicated at the 36 s stage.


The great expansion of the mesencephalon does not involve the portion immediately adjacent to the hind-brain, which is henceforth known as the isthmus (Figs. 87, 88).

The Rhombencephalon (Primary Hind-brain)

Two divisions of the embryonic brain arise from the rhombencephalon, viz., the metencephalon and the myelencephalon; the former becomes the region of the cerebellum and pons of the adult brain, and the latter the medulla oblongata. The metencephalon is a relatively short section of the original rhombencephalon, and includes only the most anterior neuromere of the rhombencephalon or the sixth of the series (Fig. 83 D, E). It may be distinguished at the beginning of the period under consideration by the fact that its roof remains as thick as that of the mesencephalon. At the end of this time, i.e., seventy-two hours, the roof in sagittal sections appears to rise sharply from the isthmus and thins towards the summit, where it passes into the thin epithelial roof of the myelencephalon (Figs. 87 and 88). The rudiment of the cerebellum is slightly thicker on each side of the middle line at seventy-two hours.

The myelencephalon becomes sharply characterized by the thinness of its roof and thickening of ventral lateral zones and floor. The epithelial roof has a triangular form, the base resting against the metencephalon. The neuromeres remain very distinct (Figs. 83, 89), but change their form. Up to about twenty-three somites they still form external expansions, but as the wall thickens the external surface becomes smooth, and the neuromeres may now be recognized as a series of concavities in the lateral wall, with intervening projections (Fig. 89). The arrangement of the nuclei leaves thin non-nucleated strips (septa) between adjacent neuromeres. The interneuromeric projections are most pronounced laterally and fade out dorsally and ventrally.

Behind the neuromeric portion of the hind-brain is a portion extending to the posterior end of the fourth mesoblastic somite from which the twelfth cranial nerve arises.

The Neural Crest and the Cranial and Spinal Ganglia

The cranial and spinal ganglia owe their origin to a structure known as the neural crest, which is a practically continuous cord of cells, hung on each side in the angle between the neural tube and the ectoderm, extending from the extreme anterior to the posterior end. Like other meristic structures the anterior portion of the neural crest is the first to arise (at about 6-7 s stage), and the remainder appears in successive order during or shortly after the closure of the neural tube in each region; thus it is not until after the completion of the neural tube that the last portion of the neural crest is established.

Fig. 89. — Frontal section of the hind-brain region of an embryo of about 36 s. Ot., Otocyst. N. 6, N. 7, N. 8, N. 9, N. 10, N. 11, Neuromeres, 6 to 11, according to Hill's enumeration, s. 1, s. 2, s. 3, First, Second, and third somites. V, Primordium of the trigeminus. VII-VIII, Primordium of the acustico-facialis.

But before this time successive enlargements of the cranial part of the crest have formed the primordia of the cerebral ganglia, and similar successively arising enlargements of the parts of the crest opposite the mesoblastic somites form the rudiments of the spinal ganglia. The intervening portions of the crest form the so-called interganglionic commissures, which subsequently appear to form mesenchyme. The formation of mesenchyme from certain parts of the neural crest is most marked in the region of the brain.

The primordia of the gangUa contain the cells (neuroblasts) which form the dorsal root fibers of the spinal nerves and parts of certain cranial nerves. They also appear to contain the cells from which the sheaths of the nerve fibers are formed; thus three kinds of cells at least are found in the neural crest, viz., mesenchyme forming cells, neuroblasts, and sheath cells.

The Cranial Neural Crest and its Derivatives

The neural crest in the head may be divided into pre- and post-otic divisions, and these arise at different times.

Fig. 90. — Transverse section of the fore-brain, and optic vesicles at the stage of 7 s. M'ch., Mesenchyme, n. Cr., Neural crest. Ph., Pharynx. Sut. cer., Anterior cerebral suture. X., Mass of cells in which the anterior end of the intestine, the neural tube and the notochord fuse.

(1) The pre-otic division, which extends from the extreme anterior end of the neural tube to about the center of the auditory pit, is well developed at a stage of 7-8 somites, but it is not found at the 5 s stage. The origin is everywhere the same, viz., from the dorsalmost cells of the medullary plate and the ectoderm immediately adjacent; it arises at the time of contact of the medullarv folds and is thus thickest in the region of the suture. Fig. 90 is a section through the developing optic vesicles, and shows the neural crest continuous with the tube and ectoderm in the neural suture; it is separated from the mesenchyme in the region of the fore-gut by a considerable space. (We shall call the latter portion of mesenchyme the axial mesenchyme of the head, to distinguish it from the mesenchyme derived from the neural crest, which later lies lateral to it, and which may thus be known as the periaxial layer.) The crest may be followed anteriorly to the extreme tip of the neural tube, and posteriorly to the region of the anterior intestinal portal, which lies at about the transverse level of the future auditory pit (cf. Fig. 91). In the region of the mid-brain it spreads out laterally until its peripheral cells reach the axial mesenchyme.

Goronowitsch divides the pre-otic portion of the neural crest into primary and secondary ganglionic crests, the post-otic portion being the tertiary crest. According to his account there is a decided difference in time of origin of the primary and secondFiG. 91. - Diagram of the cephalic ^ry crests ; the primary, involving the neural crest of a chick of about region of fore- and mid-bram, aris12 s. (After Wilhelm His.) ing before the secondary which in cludes the region of the trigeminus and acustico-facialis. I have not, however, found such a difference in my preparations.

At the stage of 10 somites the cells of the pre-otic neural crest have lost their connection with the neural tube. Behind the optic vesicles they have spread out laterally between the axial mesenchyme and the ectoderm, where they form a practically continuous periaxial layer, distinguishable from the axial mesenchyme by its greater density, and hence deeper stain; but apparently mingling with it at the surface of contact.

In the stages immediately following (10-20 s), the portions of the periaxial layer lying above the mandibular and the hyoid arches condense and thicken, and form strong cords extending from the superior angles of the neural tube into the arches in question; here they form connections with the ectoderm of the arches, which proliferates so as to contribute to their substance (Fig. 92). Elsewhere the periaxial layer gradually merges with the axial mesenchyme. The periaxial cords are the primordia of the trigeminus and acustico-facialis ganglia, and mark the paths of the trigeminal and facial nerves. Their connection with the ectoderm in the neighborhood of the first visceral pouch must not be confused with the so-called branchial sense-organs, for the primary connection is soon lost, and secondary connections arise at about the 27 s stage, and constitute the true branchial sense-organs of these arches.

Fig. 92. — Transverse section immediately behind the first visceral pouch of a chick embryo of thirteen somites. (After Goronowitsch.) Note connection of the periaxial cord with the ectoderm of the visceral arch.

Ad., Aorta descendens. c. Rounded mesenchyme cells, g. Place where cells derived from neural crest unite with the mesenchyme cells of the periaxial cord. f. Fusion, p. Spindle-shaped peripheral mesenchyme cells.

The acustico-facial periaxial cord attains definite ness some time before the trigeminal (cf. Fig. 71), and indeed appears almost from the first as a specially strong part of the periaxial layer: whereas in the region of the trigeminus the cells of this layer are first Avidely dispersed and secondarily aggregate, between the stages of 14 and 18 somites. Both cords are attached to the brain, the trigeminus to the first neuromere of the myelenoephalon, and the acustico-facialis to the third (Fig. 83 E).

The trigeminal and facial periaxial cords are supplemented, as we have seen, by proliferations of the ectoderm on each side of the first visceral pouch; the trigeminal cord then enters the mandibular arch, and the facial the hyoid arch, and in the stages between 20 and 27 somites form at least part of the mesenchyme of these arches. The axial mesoblast likewise contributes to the mesenchyme of these arches, and it becomes impossible in later stages to separate these two mesenchymal components. The ganglia proper differentiate from the upper portions of the cords. The trigeminal periaxial cord divides over the angle of the mouth and sends out a process into the rudimentary maxillary process. A third projection of the same cord towards the eye forms the path of the ophthalmic division of the trigeminus (Fig. 117).

At the stage of about 27 s the trigeminus forms a connection with a thickening of the ectoderm (placode of the trigeminus) situated in front of and above the first visceral cleft; and the facial connects similarly with a larger ectodermal thickening (placode of the facialis) situated on the posterior margin of the uppermost part of the first visceral furrow. These ectodermal thickenings are rudimentary structures of very brief duration, representing parts of the sensory canal system of the head of aquatic vertebrates. Their occurrence in the chick is an interesting example of phylogenetic recurrence. A third and fourth like organ arises in connection with the post-otic ganglia.

At the stage of 72 hours there are two ectodermal thickenings (placodes) in connection with the trigeminus, one in front of the other, derived probably by division of the original first. The facialis placode is more fully developed.

(2) The post-otic ganglionic crest is a direct continuation of the pre-otic behind the ear, and it is at first difficult to make an exact boundarv between them. At the stage of 13 s the pre-otic crest extends beneath the auditory epithelium nearly to its middle in the form of a thick mass of cells in the roof of the neural tube. Towards the posterior end of the auditory epithelium the crest becomes smaller, and this is the beginning of the post-otic crest. Behind the ear the crest becomes larger again and extends laterally so as to form a periaxial layer between the ectoderm and the axial mesoblast which extends back, above the first, second, and third somites to the middle of the fourth. The part between the ear and the first somite is, however, by far the best developed, the continuation behind being a relatively slight cord of cells.

At about the stage of 17 somites the anterior part of the crest condenses to form a well-defined periaxial cord, which arises from the neural tube above the middle of the auditory pit, arches back behind its posterior margin and extends down into the third visceral arch, where it enlarges. This is the glossopharyngeal periaxial cord. There is an enlarged jwrtion of the crest just behind this overlying the site of the future fourth and fifth arches, but its substance is not yet condensed to form a distinct periaxial cord.

At the stage of 20 somites the anterior cardinal vein and the duct of Cuvier form the posterior boundary of the enlarged portion of the post-otic crest (Fig. 73). The part of the periaxial layer immediately in front of this is somewhat condensed to form the periaxial cord of the vagus, and this is only indistinctly separated from that of the glossopharyngeus.

The formation of the third visceral cleft definitely splits the periaxial layer into the periaxial cords of the glossopharyngeus and vagus (25 s). This division is carried up indistinctly, at first, into the roots which occupy the space between the auditory sac and the first somite. The formation of the fourth visceral pouch similarly divides the distal portion of the vagus cord, so that part of it lies in front of the pouch and part behind.

At the stage of seventy-two hours the ganglion petrosum (glossopharyngeus) is definitely formed by an enlargement of the cord just above the third visceral arch, and the ganglion nodosum (vagus), similarly formed from the vagus cord, lies above the fourth visceral pouch, thus extending over the fourth and fifth arches. Branchial sense organs are formed at the dorsal angles of the second and third visceral furrows in connection with the IX and X nerves respectively.

It would appear that the neural crest in the head is the source of much of the mesenchyme, and it is an interesting question whether or not such mesenchyme has a different fate from that of different origin. Nothing definite, however, is known in regard to this, owing to the impossibihty of separating the various kinds after they have once merged.

The Neural Crest in the Region of the Somites

The neural crest is very sUghtly developed in the region of the first five somites, which is correlated with the fact that these somites are devoid of ganglia. But the mode of origin is the same throughout the somitic region. Shortly after the closure of the neural tube in any region the neural crest forms an aggregation of cells in the roof, more or less sharply separated from the remainder of the tube both by the arrangement of the cells and also by their lighter stain (Figs. 107, 109, 112, 113). The early history may be followed in a single embryo, by comparing the conditions opposite the last somite with that of more anterior somites where development is more advanced. Figs. 107, 108, 109, 110 represent transverse sections through the twenty-ninth, twenty-sixth, twentieth, and seventeenth somites of a 29 s embryo. In Fig. 107 the cells of the crest are extending towards the upper angle of the somite, with which they are connected by protoplasmic strands. The aggregation in the roof of the neural tube is thus decidedly diminished; the lateral wings of the crest lie in the angle between the neural tube and the ectoderm. In the twenty-sixth somite (Fig. 108) the lateral wings extend farther from their point of origin, and appear to have a more intimate connection with the myotome. In the more anterior and older somites, twenty and seventeen (Figs. 109 and 110), the process has progressed much farther and the neural crest cells are completely expelled from the neural tube, which closes after them (Fig. 110). A j-et later stage is shown in Fig. Ill, through the twenty-third somite of a 35 s embryo.

The dorsal commissure uniting the right and left sides of the crest ruptures, and the cells of the crest aggregate so as to form a pair of ganglia in each somite. Thus, although the neural crest is primarily a median structure, it becomes divided into two lateral halves, and although it is primarily a continuous structure it becomes divided into a series of pairs of metameric ganglia. The fate of the interganglionic commissures is conjectural. The ganglia are ill-defined from the mesenchyme when they are first formed, but they rapidly become well differentiated.

Fig. 93. — Entire embryo of 27 s viewed as a transparent object from above.

a. a. 1, a. a. 2, a. a. 3, First, second, and third aortic arches. Car., Carotid loop. Ret., Retina. V. C. 1, V. C. 2, First and second visceral clefts. Other abbreviations as before, x 20.

IV. The Organs of Special Sense (Eye, Ear, Nose)

Embryologically a sharp distinction must be drawn between the essential percipient part of the organs of sense (retina of the eye, olfactory epithelium, and epithelium of the membranous labyrinth) and the parts formed for protection and for the elaboration of function. The sensory part proper is the first to arise in the embryo, and is protected later by modifications of surrounding tissues or parts. We may thus distinguish between primary and secondary parts in the case of all organs of sense. Only the early history of the primary parts falls within the period covered by this chapter, except the formation of the lens in the case of the eye.

The Eye

The primary optic vesicles arise, as we have seen, as lateral expansions of the anterior end of the neural tube; their position is indicated by an enlargement of the neural tube even before the meeting of the medullary folds in this region. The shape and relations of the early optic vesicles have already been described and figured. The cavity may be called the Ventriculus opticus. The origin of the optic stalk by constriction of the base of the vesicle was described in a preceding section of this chapter (p. 149). The stalks remain attached to the ventral end of the lateral walls of the diencephalon in the region of the recessus opticus, and constitute tubular connections between the vesicles and the brain, in the walls of which the optic nerve develops later (Fig. 84).

Locy found six pairs of " accessory optic vesicles " occurring in series immediately behind the true optic vesicles; they form low rounded swellings of the side-walls of the neural folds before the true brain vesicles are indicated, and last only about three hours in the chick (twenty-fourth to twenty-seventh hours of incubation). "Their existence supports the hypothesis that the vertebrate eyes are segmental, and that the ancestors of vertebrates were primitive)}' multiple-e3'ed. (Locy.)

The external surface of the optic vesicle early reaches the ectoderm, to which it appears to be cemented at the 10 s stage. In the 17-18 s stage, the optic vesicles project decidedly behind the attachment of the optic stalk, and the external wall is slightly thicker than that next the brain. . The ectoderm then becomes thickened over a circular area in contact with the optic vesicle and this constitutes the primordium of the lens (Fig 94). The thickening of the external wall of the optic vesicle and of the lens primordium now proceed rapidly, and soon an invagination is formed in each (Fig. 95).

Fig. 94. — Section through the primordium of the eye of a chick embryo of 21 s. (After Froriep.)

d., Distal wall of optic vesicle, p., Proximal wall of optic vesicle.

Fig. 95. — Section through the primordium of the eye of a chick embryo at the end of the second day of incubation. (After Froriep.)

It is probable that a stimulus is exerted by the optic vesicle on the ectoderm with which it is in contact, causing it to thicken and become the primordium of the lens. This has been demonstrated experimentally to be the case in the embryo of the frog, and the morphological relations are the same in the chick. The invagination of the primary optic vesicle to form the secondary optic vesicle is not mechanically produced by the growth of the lens, as some have supposed, for it has been shown (see Fol and Warynsky) that the secondary optic vesicle is formed in the absence of the lens.

We may now consider the formation of the optic cup and of the lens separately.

The Optic Cup

The invagination of the outer wall of the primary optic vesicle gradually brings this wall into contact with the inner wall and obliterates the primary cavity. Thus is established the secondary optic vesicle or optic cup (aipula optica). Special attention must be given to the form of the invagination, for this determines relations of fundamental importance. The invagination may be stated to consist of two parts. The first is directly internal to the lens primordium, and the second, which is continuous with the first, involves the ventral wall of the primary optic vesicle as far as the optic stalk. Two parts may thus be distinguished in the mouth of the optic cup — (1) an external part, which becomes the pupil of the eye, and (2) a ventral part, continuous with the pupil, which is known as the choroid fissure. Figs. 96 A, B, and C exhibit these relations better than a detailed description.

The choroid fissure is a transitory embryonic structure, subsequently closing by fusion of its lips. However, it establishes a relation of fundamental importance in that the ventral wall of the optic-stalk is kept continuous in this way with the inner or retinal layer of the secondary optic vesicle (Figs. 96 B, and 97), and thus a path is provided for the development of the optic nerve (see Chap. IX). It also provides an aperture in the wall of the optic cup for the entrance of the arteria centralis retinae.

The optic primordium at the 36 s stage, with the omission of the lens, is composed as follows:

(1) Optic-stalk attached to the floor of the brain; this is still tubular.

(2) The optic cup or secondary optic vesicle consisting of two layers, viz., (a) a thick internal or retinal layer continuous at the pupil and choroid fissure with {b) the thin external laj^er. The cavity of the cup is the future posterior chamber of the eye; it has two openings, viz., the pupil filled by the primordium of the lens, and the slit-like choroid fissure extending from the pupil to the optic stalk along the ventral surface. The retinal layer is continuous with the floor of the optic-stalk, and thus with the diencephalon.

The optic cup expands with extreme rapidity between the stages of 26 and 36 somites, as may be seen from the figures by comparing the relative size of the lens and optic cup at different stages.

The Lens

The invagination of the thickened ectoderm external to the optic vesicle soon leads to the formation of a deep, thick-walled pit which rapidly closes (26-28 somites) and thus forms an epithelial sac, which at first practically fills the cavity of the optic cup. However, it very soon becomes detached from the posterior wall of the optic cup, which expands with great rapidity, and the lens is left at the mouth of the cup. The walls of the lens sac are at first of practically even thickness (28 s), but by the 35 s stage a great difference has arisen by the elongation of the cells of the inner wall, which are destined to form lens fibers: the cells of the anterior (outer) wall elongate much less during this period, and are destined to form the ei^ithelium of the lens (Fig. 97). Intermediate conditions are found around the equator of the lens. The subsequent history is given in chapter IX.

The Auditory Sac

At about the 12 s stage the first evidence of the auditory sacs is found in the form of a pair of circular 23atches of thickened ectoderm situated on the dorsal surface of the head opposite to the ninth, tenth, and eleventh neuromeres, and thus a short distance in front of the first mesoblastic somite; it lies between the rudiments of the acustico-facialial and glossopharyngeal ganglia. In the 14 s stage the auditory epithelium is slightly depressed, and in the 16 s stage it forms a wide-open pit. At about the 20 s stage the mouth of the pit narrows slightly, and gradually closes (28-30 s), thus forming the auditory sac or vesicle (otocyst) (cf. Figs. 71, 73, 89, and 93).

Fig. 97. — Transverse section through the eyes and heart of an embryo of about 35 s. The plane of the section will be readily understood by comparison of Fig. 117.

ch. Fis., Choroid fissure. D. C, Duct of Cuvier. Lg., Lung. pi. gr., Pleural groove. V. c, Posterior cardinal vein. Y. S., Yolk-sac. Other abbreviations as before.

The method of closure of the pit, which is of interest, may readily be observed in mounts of entire embryos; at first the lips fold over most rapidly from the anterior and posterior margins; thus the mouth of the pit becomes elliptical with the long axis vertical (stage of 22 somites) and extending from the apex nearly to the base. The ventral lip then begins to ascend (stage of 24 somites) and the closure gradually proceeds towards the apex, so that by the stage of 29 somites the opening is reduced to a minute eUipse situated on the external side of the dorsalmost portion of the otocyst (see Fig. 93). This portion of the otocyst now begins to form a small conical elevation, and the final closure takes place on the external side of this elevation, which is destined to form the endolymphatic duct. The latter remains united to the epidermis at this point for a considerable period of time by a strand of cells which may preserve a lumen up to 104 hours (Fig. 98). The final point of closure of the otocyst is thus very definitely placed, and it coincides with the middle of the endolymphatic duct, that is, with the junction of the later formed saccus and ductus endolymphaticus. In the Selachia this duct remains in open communication with the exterior throughout life; the relatively long persistence of its connection with the epidermis in the chick may thus be interpreted as a

Fig. 98. — Section of the otocyst phylogenic reminiscence of the an- of an embryo of 104 hours. The , i-^. original opening of the otocyst

cestral condition. .\

The Nose (Olfactory Pits)

At ^^.^j ...^j^h connects with the about the 28 s stage, the ectoderm endolymphatic duct (recessus on the sides of the head a short dis- labyrinthi).

i^noP' in front of the eves aDDears otocyst

tance m iiom oi ine eyes appeaib (.^^^jj^^.,)^ b., Canalleading from

thickened. Two circular patches of the surface to the otocyst. D.

ppfnrlprm nrp thus marked off the end'l., Endolymphatic duct. D., ectoderm are tnus maiKea on,^ me j^^^^^^j ^^^^ Ectoderm of the

beginning of the olfactory epithe- surface of the head. Gn., Audi lium; at first this grades almost im- tory ganglion. L Lateral. M.,

' '^ . , , . Median. V., ventral,

perceptibly into the neighboring ectoderm. In the stages immediately following the olfactory plates appear to sink down towards the ventral surface of the head, due no doubt to more rapid growth of the dorsal portion of the head. Thus they appear at the ventro-lateral angles of the anterior part of the head at the stage of 36 somites. During the displacement a depression appears in the center of each olfactory plate, and as this becomes deeper, the olfactory pits are formed (Figs. 99 and 117). At the stage of 36 somites each is a deep pit situated at the junction of the sides and ventral surface of the anterior portion of the head, with the wide mouth opening outwards and ventrally.

The olfactory epithelium now becomes sharply differentiated from the ectoderm of the head, owing to the formation of a superficial la3^er of cells (teloderm, see p. 285) above the columnar cells in the ectoderm, but not in the region of the sensory epithelium, where the cells still form a single layer. In the center of the olfactory pit the epithelium is very much thickened owing to elongation of the cells, and the nuclei lie in five or six layers; there is a gradual thinning of the epithelium to the lips of the pit and then a sudden, but graduated, decrease to the general ectoderm. The line of junction of olfactory epithelium and indifferent ectoderm of the head is a little distance beyond the margin of the pit, as may be determined by the edge of the telodermic layer; in other words, all of the olfactory epithelium is not yet invaginatecl.

It is probable that the invagination of the olfactory plates is due mostly, up to this time, to the processes of growth within the plates themselves, although there has been considerable accumulation of mesenchyme in this region. But the subsequent deepening of the pits appears to be due largely to the formation of processes around the mouths of the primary pits. (See Chap. IX.)

V. The Alimentary Tract and Its Appendages

We have already learned that the main portion of the alimentary tract arises from the splanchnopleure; a portion of the mouth cavity is, however, lined with ectoderm and arises from an independent ectodermal pit, the stomodceum, which communicates only secondarily with the entodermal portion; similarly the last portion, external to the cloaca, arises from an ectodermal pit, the proctodceum, which communicates only secondarily with the entodermal part. We shall thus have to consider the origin of the stomodseum and the proctodeum in connection with the alimentary tract.

Fig. 99. — Entire embryo of 31 somites viewed as a transparent object, am. Umb., Amniotic umbilicus. B. a., Bulbus arteriosus, cerv. Fl., Cervical flexure, ch. Fis., Choroid fissure, cr. Fl., Cranial flexure. D. C, Duct of Cuvier. ex. o. c, External layer of the optic cup. int. o. c, Internal layer of the optic cup (retina.) N'm., Neuromere of myelencephalon. olf., Olfactory pit. pc. W., Line of attachment of amnion to pericardial wall. V. C. 1, 2, 3, First, second, and third visceral clefts. Other abbreviations as before.

From the embryological point of view the aUmentary tract may be divided into fore-, mid-, and hind-gut. The fore-gut inchides the anterior portion as far back as the hver diverticula, the mid-gut extends from here to the coecal appendages, and the hind-gut inchides the remainder. From each division there arise certain outgrowths which may be termed collectively appendages of the alimentary tract, and these will also be considered here, so far as they arise within the period covered by this chapter. Thus from the fore-gut there arise the visceral pouches, the thyroid and thymus glands, the postbranchial bodies, the respiratory tract, and the liver and pancreas; from the mid-gut the 3^olk-sac, and from the hind-gut the ccecal appendages and allantois.

The enlargement of the body-cavity towards the middle line gradually reduces the broad mesodermal septum situated between its inner angles to a relatively narrow plate, which forms the dorsal mesentery of the intestine (Figs. 107, 109, 110, and 111). This elongates in the course of development and forms a sheet of tissue suspending the intestinal tube to the mid-dorsal line of the bodycavity. It is composed of two layers of mesothelium (peritoneum) continuous with the lining of the body-cavity and enclosing a certain amount of mesenchyme; the dorsal mesentery extends along the entire length of the intestinal canal.

A ventral mesentery uniting gut and yolk-sac is also established by the meeting of the limiting sulci in the splanchnopleure. When the body-wall closes, the ventral mesentery consists of two layers of mesothelium attaching the intestinal canal to the mid-ventral line of the body-wall. The dorsal and ventral mesenteries, together with the alimentary canal, thus constitute a complete partition between the right and left halves of the bodycavity. However, the ventral mesentery is a very transient structure except in the region of the fore-gut and liver, and in the extreme end of the hind-gut. In these places it is persistent and is the seat of formation of important organs.

The wall of the intestine contains three embrvonic lavers: viz., entoderm, mesenchyme, and mesothelium. The first forms the lining epithelium of the intestine, and of all glandular attachments, as well as of the respiratory tract and allantois; the last forms the serosa; and the mesenchyme the intermediate layers.

We shall now consider the development of each region of the alimentary tract and the appendages proper to each in the following order: (1) Stomodseum, (2) Pharynx, (3) CEsophagus, (4) Stomach, (5) Hepato-pancreatic division of the fore-gut, (6) Midgut, (7) Hind-gut.

The stomodaeum owes its origin to an expansion of the embryonic parts surrounding the oral plate, and it gives rise to a large part of the buccal cavity, which is therefore lined by ectoderm. (See Chap. X.) It will be remembered that at the 12 s stage the oral plate lies between the pericardium and the forebrain (Fig. 67), and that it consists of a fusion between the ectoderm of the ventral surface of the head and the entoderm composing the floor of the anterior end of the fore-gut. It lies in a slight depression on the under surface of the head which is the beginning of the oral cavity. This small beginning owes its enlargement (1) to the cranial flexure, by which the ventral surface of the head becomes bent at right angles to the oral plate instead of forming a direct continuation of it, and (2) to the formation and protrusion of the mandibular arches and maxillary processes at the sides and behind. (See fuller account in Chap. VII.) In this waj' it becomes a deep cavity closed internally by the oral plate. The series of figures of sagittal sections through the head illustrates very well the gradual deepening of the stomodseum by these processes (Figs. 75, 85, 87, 88).

The oral plate thins gradually from the 12 to the 30 s stage when it breaks through (Figs 87 and 88), thus establishing an opening into the alimentary tract. The remnants of the oral membrane then gradually disappear and leave no trace. The subsequent extension of the maxillary region to form the upper jaw greatly enlarges the extent of the ectodermal portion of the buccal cavity. It will have been noted (Figs. 85 and 87) that the hypophysis opens in front of the oral plate on the ectodermal side, and this constitutes a most important landmark for determining the limit of the ectodermal portion of the buccal cavity in later stages.

The Pharynx and Visceral Arches

The pharynx may be briefly defined as the alimentary canal of the head. It is the most variable part of the alimentary canal in the series of vertebrates. ]\Iodified, as it is in all vertebrates, for purposes of respiration, the transition from the aquatic to the terrestrial mode of respiration brought about great changes in it. It is thus marked embryologically first by the development of structures, the visceral arches and clefts, whose primary function was aquatic respiration, and second by the development of the air-breathing lungs. Such fundamental changes in function have left a deep impression, not only on the embryonic history of the pharynx itself, but also on the development of the nervous and vascular systems.

The extreme anterior end of the pharynx extends at first some distance in front of the oral plate, and may hence be called the pre-oral gut (Figs. 75, 85, etc.). After the rupture of the oral plate, the pre-oral gut appears like an evagination of the pharynx immediately behind the hypophysis and is now known as Seessel's pocket (Fig. 87), but it gradually flattens out and disappears (Fig. 88).

The form of the pharynx at thirty-three hours has l^een already described; briefly, it is much expanded lateralh^, exhibiting a crescentic form in cross-section (Fig. 54 A). The horns of the crescent are in contact with the ectoderm in front of the auditory pit, marking the site of the future hyomandibular cleft, which arises by perforation in the fused area at about forty-six hours. A second pair of lateral expansions brings about a second fusion of the lateral wings of the pharynx just behind the auditory pit at about the stage of 19-20 somites. This is followed b}^ the formation of a third and a fourth pair of lateral evaginations of the pharynx which reach the ectoderm at about 23 s and 35 s respectively. The walls of the pharynx appear considerably constricted between the evaginations which are known as visceral pouches (Figs. 100 and 101).

Corresponding to each visceral pouch there is formed an ectodermal invagination of much lesser extent, which may be known as the visceral furrow. The furrows do not form directly opposite the pouches, but slightly behind them so as to overlap the margins of the latter (Fig. 101). The ectoderm of the visceral furrows forms a close union with the entoderm of the pouches, and openings arise within these areas, excepting the fourth, forming transitory visceral clefts.

There are thus four pairs of visceral pouches and furrows, known as the first, second, third, and fourth; the first is sometimes called the hyomandibular.

According to Kastschenko, there are evidences of three pairs of visceral furrows in front of the first at the 14-16 s stage. These he interprets as phyletic rudiments. It is certain that the lower vertebrates had pouches posterior to the fourth. The post-branchial bodies (see p. 309) are probably rudiments of a fifth pair of pouches.

The tissue between the visceral pouches thickens, by accumulation of mesenchyme, to form the visceral arches, of which there are five, viz.: (1) the tnandibular in front of the first pouch, forming also the posterior boundary of the oral cavity, (2) the hyoid between the first and second pouches, (3) the third visceral arch between the second and third pouches, (4) the fourth visceral arch between the third and fourth pouches, and (5) the fifth visceral arch behind the fourth pouch. Each arch is bounded internally by entoderm, externally by ectoderm. The main portion of its substance is formed of mesenchyme; each contains also a branch of the ventral aorta (aortic arch) and a branch of a cranial nerve. TTnderstanding of their relations is therefore essential to knowledge of the development of the nervous system, vascular system, and skull.

Fig. 100. — Reconstruction of the fore-gut of a chick of 72 hours. (After Kastschenko.)

Hyp., Hypophysis, lar-tr. Gr., Laryngotracheal groove. Lg., Lung. Md. a., Mandibular arch. Oes., Oesophagus, pr'o. G., Preoral gut. Stom., Stomach. Th., Thyroid, v. C. d, 1, 2, Dorsal division of the first and second visceral clefts, v. C. v. 2, Ventral division of the second visceral cleft, v. P. 1, 2, 3, 4, First, second, third, and fourth visceral pouches.

We shall now consider the history of each visceral pouch and arch separately:

The first visceral pouch becomes adherent to the ectoderm of the first visceral furrow at its dorsal and ventral ends, leaving an intermediate free portion. At about the 26 s stage an opening (cleft) forms at the dorsal adhesion, but none at the ventral; thus the first visceral cleft is confined to the dorsalmost portion of the pouch (Fig. 100). This opening closes about the end of the fourth day; the ventral portion of the pouch then flattens out, and the dorsal portion expands upwards towards the otocyst (Fig. 102).

The first visceral (mandibular) arch thickens greatly between the 14 and 35 s stages, the ventral ends project a little behind the oral invagination, and subsequently meet to form the primordium of the lower jaw (Figs. 125 and 126, Chap. VII). A projection of the upper anterior border just behind the eye is the beginning of the maxillary process, or primordium of the maxillary portion of the upper jaw.

Fig. 101. — Frontal section through the pharynx of a 35 s embryo. a. a. 1, 2, 3, 4, First, second, third, and fourth aortic arches. Hj-p., An

terior lobe of the Hypophysis. J., Jugular vein, branchial portion of pharynx. Ph., Pharj-nx 3, First, second, and third visceral arches. F. 2, 3, Second and third visceral furrows.

or., Oral cavitv. p. br., PostTh., Thyroid, v. A. 1, 2,

v. C. 1, First visceral cleft. V. P. 2, 3, 4, Second, third. and fourth visceral pouches. HI, Third cranial nerve.

The second visceral pouch likewise becomes adherent to the ectoderm of the second visceral furrow at its dorsal and ventral ends, and openings are formed in each adhesion by the 35 s stage (Fig. 100) ; the dorsal opening is small and oval (later becoming more elongated) while the ventral one is a long, narrow fissure; they are separated only by a narrow bridge of tissue, and close during the fourth day.

The third visceral pouch behaves like the second, forming a small round dorsal, and long fissure-like ventral cleft at about the 40 s stage (Fig. 102). These close during the fifth day.

The significance of the separate dorsal and ventral divisions of the visceral clefts is an interesting question. It is probable that the dorsal division had a special function, as they have a special connection with the branchial sense organs.

Fig. 102. — Reconstruction of the pharyngeal organs of the chick at the end of the fourth day of incubation. (After Kastschenko.) a. a. 3, a. a. 4, a. a. 6, Third, fourth, and sixth aortic arches. Car. e., External carotid. Car. i.. Internal carotid. G. Gn., Geniculate ganglion. G. n. X., Ganglion nodosum. G. pr.. Ganglion petrosum. ot., Otocyst. p. A., pulmonary artery. Th., Thyroid, v. P. 1, 2, 3, 4, First, second, third, and fourth visceral pouches.

V, VH, VIII, IX, X, XII, Cranial nerves and ganglia.

The fourth visceral pouch connects with the ectoderm at its dorsal end, about the 35 s stage, but no cleft develops. Its posterior wall develops an evagination (postbranchial body) which by some is considered to be a rudimentary fifth pouch, and which contributes to the formation of the thymus. (See Chap. X.)

The second visceral arch is the largest of the arches and overlaps both the first and third. See Figs. 117 and 125 in place of description. All of the arches are wedge-shaped, corresponding to the wedge-like form of the hind-brain region. The fourth arch is small and incomplete ventrally; the fifth a mere transitory rudiment. The greatest development of the arches is at about the end of the fourth day.

According to Kastschenko the closure of the visceral clefts takes place external to the meeting-place of the visceral furrows and clefts, and in this way some of the ectoderm of the furrows remains attached to the visceral pouches.

The thyroid arises as a small, spherical evagination of the epithelium of the floor of the pharynx situated between, and a little in front of, the ventral ends of the second pair of visceral pouches (Figs. 85, 87, 88, 101). In the 18-20 s stage, it is represented by a sharply defined plate of high, columnar cells in the same situation, which may be recognized even at the stage of 12 s. At the stage of 26 s this plate forms a deep, saucer-shaped depression, and at the 30 s stage it is a well-developed sac with wide-open mouth which gradually closes, thus transforming the sac into a small spherical vesicle lying beneath the floor of the pharynx (Fig. 102).

The Pulmonary Tract

The portion of the pharynx that includes the visceral pouches may be called the branchial portion, because it is homologous to the gill-bearing portion in fishes and amphibia, and because the visceral pouches are phylogenetic rudiments of branchial clefts. The larnyx, trachea, and lungs develop from the ventral division of the postbranchial portion of the pharynx. At about the 23 s stage a reconstruction shows this respiratory division of the pharynx slightly constricted from the broader branchial portion, enlarged on each side at its posterior end and with a ventral depression; the latter rapidly deepens to form a narrow groove, the primordium of the larynx and trachea, while the posterior lateral expansion begins to form outgrowths, the primordia of the lungs and air-sacs. By the stage of 35 s (Fig. 100) the postbranchial portion of the pharynx has become narrow transversely and its ventral half is a deep groove (laryngotracheal groove) leading back to the lung primordia. A true median sagittal section at this time shows the floor of the laryngotracheal groove directly continuous with the floor of the branchial portion of the pharynx at its hind end; the former bends up at about right angles to enter the narrow oesophagus (Figs. 87 and 88).

Thus the whole pulmonary tract communicates widely with the pharynx at the 35 s stage. Its complete delimination falls within the period covered by Chapter X. The continuity of the expansions that form the lung primordia, with the series of visceral pouches as shown in Fig. 100, is especially noteworthy ^s suggesting a theory of the phylogenetic derivation of the lungs.

Fig. 103. — Reconstructions of the liver diverticula of the chick. (After Hammar.)

A. On the third day of incubation; from the left side; the diverticula arise from the anterior intestinal portal.

B. Beginning of the fourth day; from the left side.

a. i. p., Anterior intestinal portal. D. V., Indicates position of ductus venosus. g. b., Gall bladder. 1. d. d. (cr.)., Dorsal or cranial liver diverticulum. 1. d. v. (caud.), Ventral or caudal liver diverticulum, pc. d., Dorsal pancreas. X., Marks the depression in the floor of the duodenum from which the common bile duct is formed.

(Esophagus and Stomach. Immediately behind the pharynx, at the stage of 36 s, the intestine narrows suddenly (primordium of oesophagus) and enters a small, spindle-shaped enlargement, the primordium of the stomach (Figs. 87, 88, 100).

The liver arises in the chick as two diverticula of the entoderm of the anterior intestinal portal, one situated immediately above and the other below the posterior end of the ductus venosus, or fork of the omphalomesenteric veins (Fig. 103 A). This portion of the anterior intestinal portal becomes incorporated in the floor of the intestine as the anterior intestinal portal retreats backwards, and the original dorsal liver diverticulum therefore becomes anterior or cephalic and the ventral becomes posterior or caudal (Fig. 103 B). Before this transposition occurs, however, the diverticula have grown forward towards the sinus venosus in the ventral mesentery of the stomach, the anterior diverticulum above and the posterior diverticulum below the ductus venosus. The stretch of entoderm between the two liver diverticula thus lies in the angle made by the union of the two omphalomesenteric veins. At the stage of 26 somites, the anterior diverticulum has grown forward above the ductus venosus to the level of the Cuvierian veins and is large and flattened laterally. The posterior diverticulum is barely indicated at this time.

The anterior diverticulum was originally described as left and the posterior as right (Goette, 1867), and this description was taken up by Foster and Balfour. This was corrected by Felix (1892). Subsequent writers do not agree exactly as to the time or precise relations of the diverticula; however, it is generally agreed that the two diverticula are subdivisions of a common hepatic furrow, inasmuch as the entoderm between them lies below the level of the entoderm in front and behind (Fig. 103 B). Brouha maintains that at first the hepatic furrow lies in front of the anterior intestinal portal, and that the latter secondarily moves forward so as to include the hepatic furrow, which later again comes into the floor of the intestine with the definitive retreat of the anterior intestinal portal. This view does not rest on very secure evidence, and is probably based on interpretation of slight individual variations as successive stages of development. Choronschitzky places the time of appearance of the hepatic diverticula at about the thirty-sixth hour. It is probable, however, that this is too early. I have found the first unmistakable diverticulum at a stage of 22 somites, a slight rudiment of the anterior diverticulum in the anterior intestinal portal.

At the 30 s stage the anterior or dorsal diverticulum has expanded much more, mainly to the left of the middle line, as though to embrace the ductus venosus, and the posterior or ventral diverticulum has an even greater development and embraces the right side of the ductus venosus, but it does not extend as far forward as the anterior diverticulum. Both diverticula now branch rapidly and profusely, forming secondary anastomoses where branches meet, so that a complete ring of anastomosing columns of hepatic cylinders is rapidly formed around the center of the ductus venosus (Figs. 103 B and 104, cf. also Figs. 119 and 120). But the anterior and posterior ends of the ductus venosus are not yet completely surrounded by the basket-work of liver substance, owing to the absence of any part of the posterior diverticulum in its anterior portion, and of the anterior diverticulum in its posterior portion.

The floor of the intestine between the anterior and posterior liver diverticula is depressed; later it becomes separated from the intestinal cavity to form a temporary common bile-duct; which then receives the tw^o primary diverticula (Figs. 103 B, 104 and 187).

The pancreas arises from a dorsal and a pair of ventral primordia. The former is an outgrowth of the dorsal wall of the intestine immediately above the posterior liver diverticulum (Figs. 103 B and 104). At the 35 s stage it is a solid thickening of the dorsal wall of the intestine of considerable extent; a little later the base of the thickening is hollowed out, and the free margin sends off solid buds into the dorsal mesentery just behind the stomach. The ventral primordia arise from the posterior liver diverticulum in a manner to be described later (Chap. X).


At the 35 s stage the mid-gut is still open to the yolk-sac. Its subsequent history is given in Chapter X.

Fig. 104. — Reconstruction of the liver of the chick at the end of the fourth day of incubation. (After Hammar.)

du., Duodenum. L., Substance of liver. Other abbreviations as before.

Anal Plate, Hind-gut, Post-anal Gut, and Allantois

At about the 14 s stage a thickening of the ectoderm in the middle line just behind the primitive streak extends towards the entoderm which is folded up so as to nearly meet it, thus cutting off the extra-embryonic mesoblast from the primitive streak. The ectoderm and the entoderm then come into contact here, and form a firm union, the anal plate (Fig. 70), which is subsequently perforated to form the anus. At first, however, the anal plate lies entirely behind the embryo, and the post-anal portion of the embryo arises from the thickened remnant of the primitive streak (tail-bud) which grows backwards over the blastoderm beyond the anal plate. Even before this, however, the hind-gut begins to be formed by a fold of the splanchnopleure directed forwards beneath the tail-bud, and the hind end of the tube thus formed ends at the anal plate (Fig. 70). The entoderm in front of the anal tube is fused with the substance of the tail-bud, and as the latter grows backwards beyond the anal plate it carries with it a pocket of the hind-gut, and this forms the post-anal gut (Fig. 80).

The formation of the tail brings the anal plate on to the ventral surface of the embr3^o at the junction of tail and trunk, and the post-anal gut then appears as a broad continuation of the hind-gut extending behind the anal plate, and ending in the tail at the hind end of the notochord (Fig. 80). The further elongation of the tail draws out the post-anal gut into a narrow tube lying beneath the notochord in the substance of the tail; it then gradually disappears and leaves no trace.

The formation of the hind-gut takes place prior to the formation of the embryonic body-cavity at this place. It thus happens that the splanchnic mesoderm, forming the floor of the hind-gut, is directly continuous with the somatic mesoderm. When the body-cavity does penetrate this region it is without direct lateral connections with the extra-embryonic body-cavity, so that the connection of the splanchnic and somatic mesoderm persists, forming the ventral mesentery of the hind-gut (Fig. 81). This is a thick mass of mesoblast binding the hind-gut to the somatopleure. The hind-gut is deep from the first, and its ventral division soon begins to extend into the ventral mesentery as a broad evagination, the allantois (see p. 143).

VI. History of the Mesoderm

The history of the extra-embryonic mesoderm is considered sufficiently in the first part of this chapter. The history of the embryonic mesoderm will be considered under the following heads: (1) Somites, (2) Intermediate Cell-mass, (3) Vascular System, (4) Lateral Plate and Body-Cavity, (5) Mesoblast of the Head.

Fig. lOo. — Embryo of about 27 somites drawn in alcohol by reflected light; upper side, x 10. Am., Amnion, ot., Otocyst. t. F. Am., Tail fold of amnion.

(1) Somites. The rate of formation of the somites from the segmental plate and their number at different times is given in the normal table of embryos (p. 68), and may be seen in various figures of entire embryos. The formation of new somites continues after the end of the period discussed in this chapter, up to about the sixth day. Each somite has a definite value in the developmental history.

Fig. 106. — The same embryo Irom beiieatli. x lU.

a. i. p., Anterior intestinal portal. A. V., Vitelline artery. Int., Intestinal groove.

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, Xormaltafeln). 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. This points towards a long-tailed ancestr}- for birds.

Although the somites have the same fundamental structure in all parts of the body, they differ greatly in many respects" (Williams). It is not, however, our purpose to consider the individual characters of each pair of somites, but rather the relations common to all.

Each somite is composed of an epithelial wall of high, columnar cells, enclosing a core of cells that nearly fills the cavity (Figs. 112, 113, etc.). From each somite there arise three parts of fundamental significance, viz., the sclerotome, the muscle plate, and the cutis plate (dermatome), the primordium of the axial skeleton, the voluntary muscles (excepting those of the head), and derma respectively. The manner of origin of these parts may be studied fully in an embryo of 25 to 30 somites, by comparing the most posterior somites, in which the process is beginning, with somites of intermediate and anterior positions in the series, which show" successively later stages.

Fig. 107. — Transverse section through the last somite of a 29 s embryo.

n. Cr., Neural crest. Neph., Nephrotome. W. D., Wolffian duct. Other abbreviations as before.

Figs. 107, 108, 109, and 110 represent transverse sections through the tw'enty-ninth, twenty-sixth, twentieth, and seventeenth somites of a 29 s embrvo. In the twenty-ninth somite (Fig. 107) the primitive relations of the parts are still preserved. In the twenty-sixth somite (Fig. 108) it will be seen that the cells of the core and of the ventral and median wall of the somite extending from the nephrotome to about the center of the neural tube are becoming mesenchymal; they spread out towards the notochord and the space between the latter and the dorsal aorta. These cells constitute the sclerotome. The muscle plate extends from the dorsal edge of the sclerotome to the dorso-median angle of the w^all of the somite, and the dermatome from this point to the nephrotome.

Fig. 108. — Transverse section through the twenty-sixth somite of a 29 s embryo. (Same embryo as Fig. 107.) Derm., Dermatome. My., Myotome. Scler., Sclerotome. V. c. p., Posterior cardinal vein. Other abbreviations as before.

Fig. 109 is a section through the twentieth somite of the same embryo. The sclerotome is entirely mesenchymal, and its cells are extending between the notochord and aorta, and along the sides of the neural tube. The muscle-plate has now bent over so that its inner surface is being applied against the dermatome, but there is still a considerable cavity (myocoele) between the two, at the lateral angle of the dermo-myotomic plate. The lateral edge of the dermatome is freed from the nephrotome, and turns in to a slight extent. Other details are readily understood from the figure.

The growth of the free edge of the muscle-plate towards the free lateral edge of the dermatome continues as illustrated in Figs. 109 and 110, until complete union of the two takes place (Fig. Ill) and there is established a complete dermomyotomic plate in each somite, which therefore includes two layers: the external cutis-plate or dermatome, and the internal muscle-plate or myotome. With the elevation of the axis of the body, the dermo-myotome gradually assumes a nearly vertical position.

Fig. 110. — Transverse section through the seventeenth somite of a 29 s embryo. (Same embryo as Fig. 107.) am. Cav., Amniotic cavity. E. E. B. C, Extra-embryonic body-cavity. Gn., Ganghon. mes'n. V., Mesonephric vesicle. S.-Am., Sero-amniotic connection. Other abbreviations as before.

Other details concerning the early history of the sclerotome are given in Chapter XIII, and it remains to add here only a short description of certain changes in the cells of the myotome (mj^oblasts). In longitudinal sections the cells of the myotome are seen to become spindle-shaped soon after the folding towards the dermatome begins. The nuclei of the myoblasts are large and stain less deeply than those of adjoining tissues. They become elliptical in correspondence with the form of the cellbodies. Each myoblast soon stretches from anterior to posterior faces of the somite, and this represents the first stage in the differentiation of the voluntary muscles.

In later stages the myotomes send outgrowths into the limbbuds and ventral body-wall for the formation of the voluntary muscles of these parts. The voluntary muscles of the head, on the other hand (excepting the hypoglossus musculature), arise in front of the somites; the mesoblast from which they arise is, however, part of the original paraxial mesoblast, in large part at least. It is important to note that the voluntary muscles are epithelial in origin. The involuntary, or smooth, muscle fibers, on the other hand, are mesenchymal in origin.

The dermatome remains epithelial in all the somites well into the third day; the cells then begin to separate and form mesenchyme; this process begins at the anterior somites and proceeds backwards. The mesenchyme thus formed is the foundation of the derma.

The Intermediate Cell-mass or Nephrotome. This is the cord of cells uniting somite and lateral plate; it reaches its typical development only from the fifth to the thirty-third somites, in which it contributes to the development of the excretory system. Behind the cloaca, that is in the region of the tail, there is no lateral plate and no nephrotome.

Origin of the Excretory System

The history of the excretory system in Amniota is of particular interest, because it shows a succession of three separate organs of excretion or kidneys, the first of which is a mere functionless rudiment, the second is the principal organ of excretion during embryonic life (at least in reptiles and birds), and the third finally becomes substituted for the second, which degenerates and is mostly absorbed; however, parts of the second remain and contribute to the formation of the organs of reproduction. The first, known as the head kidney or pronephros, is probably homologous to the permanent kidney of Amphioxus; the second or mesonephros, is the homologue, in part, of the permanent kidney of Anamnia, and the third or metanephros is the permanent kidney. The secreting parts of all arise from the intermediate cell-mass, though not in the same manner. The development of the metanephros does not begin until the fourth day; it is therefore not considered in this chapter.

Pronephros and Wolffian Duct

The pronephros extends over only eleven or twelve somites, viz., from the fifth to the fifteenth or sixteenth inclusive; it consists originally of as many parts or tubules as the somites concerned. Each tubule arises as a thickening of the somatic layer of the intermediate cell mass, which grows out towards the ectoderm in the form of a bUnd, soUd sprout. The distal end of each turns backwards and unites with the one behind so as to form a continuous cord of cells, which is thus united with the intermediate cell-mass in successive somites by the original outgrowths. This cord of cells is the beginning of the Wolffian duct. Behind the sixteenth somite, the latter grows freely backwards just above the intermediate cell-mass until it reaches the cloaca with which it unites about the 31 s stage.

Fig. 112. — A. Transverse section through the twelfth somite of a 16 s embryo.

B. Three sections behind A to show the nephrostome of the same pronephric tubule.

V. c. p., Posterior cardinal vein. c. C, Central canal. Ms'ch., mesenchyme, n. Cr., Neural crest. N'st. Nephrostome. n. T., Neural tube, pr'n. 1, 2, Distal and proximal divisions of the pronephric tubule.

The primary pronephric tubules are originally attached to the nephrotome opposite the posterior portion of the somite, about half-way between the somite and the lateral plate (Figs. 112 and 113). The part of the nephrotome between the attachment of the primary tubule and the lateral plate is continuous with the primary tubule and forms a supplementary part of the complete pronephric tubule; the remainder of the nephrotome then becomes converted into mesenchyme and the connection with the somites is lost (Figs. 112 and 113). Thus each protiephric tubule forms a connection between the Wolffian duct and the angle of the body-cavity; it consists of two parts, viz., the primary tubule and the supplementary part. It never possesses a continuous lumen, though there is often a cavity in the supplementary part, which opens into the body-cavity through the nephrostome (Fig. 112 B).

The pronephros of the chick is a purely vestigial organ, of no apparent functional significance. Its development is accordingly highly variable, and it often happens that the right and left sides of the same embryo do not correspond. It is also of very short duration and is usually completely lost on the fourth day. The tubules in the fifth to the tenth somites, moreover hardly pass the first stage when they appear as thickenings of the somatic layer of the somitic stalk; thus the Wolffian duct does not extend into this region, and the best developed pronephric tubules are confined to the tenth to the fifteenth somites.

Fig. 113. — Transverse section through the fifteenth somite of the same embryo, pr'n. (14), (15), Pronephric tubules of the fourteenth and fifteenth somites, respectively.

The pronephric tubules do not form Malpighian corjDuscles; but glomeruli develop as cellular buds at the peritoneal orifices of the posterior tubules, projecting into the coelome near the mesentery. Curiously enough these do not form at the time of greatest development of the tubules, but subsequently to this when the tubules themselves are in process of degeneration. Moreover, they are extremely variable as to number, and degree of development. They appear to be best developed on the third and fourth clays. They agree in many respects with the so-called external glomeruli of the pronephros of Anamnia, and should be homologized with these. On the other hand, they appear at the same time as the first glomeruH of the mesonephros (q. v.) and possess, by way of the intermediate tubules, undeniable resemblance to the latter.

At the stage of 10 somites the pronephros is represented by a series of thickenings of the somatic layer of the intermediate cell-mass extending from the fifth somite backward to the segmental plate. In an embryo of 13 somites the connection between the somite and nephrotome is lost, and the pronephric tubules from the ninth to the thirteenth somites have united to form the beginning of the Wolffian duct.

In an embryo of 16 somites a single pronephric tubule was found at the level of the hind end of the fifth somite, and was very distinct on one side but hardly discernible on the other. Its posterior continuation was soon lost, and the next distinct tubules were between the ninth and tenth somites ; from here back there was a tubule opposite the hind end of each somite to the fifteenth, which was the last, and the duct was continuous.

In an embryo of 21 somites, one finds only isolated remnants of the pronephros in front of the eleventh somite; from here to the fifteenth the tubules are well developed and retain their connection both with the Wolffian duct and the lateral plate. The Wolffian duct extends back of this place to the region of the posterior half of the segmental plate.

At the 35 s stage the pronephric tubules are much degenerated, but the nephrostomes usuafiy remain. In one embryo there was found a well-developed pronephric tubule on each side in the thirteenth somite. That of the left side had a wide nephrostome, the lumen of which stopped short of the tubule; the nephrostome of the right side was rudimentary. On the right side the Wolffian duct extended no farther forward, but on the left side it was continued to the eleventh somite, and rudimentary pronephric strands uniting it to the coelomic epithelium existed in both eleventh and twelfth somites. Here the Wolffian duct stopped. But isolated pronephric rudiments and minute nephrostomes were found on both sides as far forward as the tenth somite.

The Wolffian Duct. The Wolffian duct consists according to the foregoing account of two parts, (1) an anterior division formed by the union of the pronephric tubules, and (2) a posterior division that arises as an outgrowth of the anterior part. The latter grows backward above the intermediate cell-mass as a solid cord (Fig. 107), apparently by active multiplication of its own cells, without participation of the neighboring mesoderm or ectoderm, until it reaches the level of the cloaca at about the sixtieth hour (30-31 s). It acquires a narrow lumen anteriorly at about the 25 s stage; but the remainder is solid. At about the sixtieth hour the ends of the ducts fuse with broad lateral diverticula of the cloaca, and the lumen extends backwards until the duct becomes viable all the way into the cloaca (at about seventy-two hours, 35 s stage).

The Mesonephros or Wolffian Body

The mesonephros develops from the substance of the intermediate cell-mass between the thirteenth or fourteenth somites and the thirtieth somite. There are slight local differences in the relations of the tubules in front and those behind the nineteenth and twentieth somites, but in general the tubules may be stated to arise as epithelial vesicles derived from the intermediate cell-mass, which become transformed into tubules, one end of w^hich unites with the Wolffian duct and the other forms a Malpighian corpuscle in the manner described below. It will be seen that the anterior mesonephric tubules which are relatively rudimentary and of brief duration overlap the posterior pronephric tubules; they may possess nephrostomes, whereas the typical mesonephric tubules formed behind them, which constitute the main bulk of the mesonephros, never possess peritoneal connections.

An embryo with 29-30 somites is in a good stage for considering the early development of the mesonephric tubules. If one examines a section a short distance behind the last somite, one finds that the intermediate cell-mass is a narrow neck of cells uniting the segmental plate and the lateral plate, and that the cells composing it are arranged more or less definitely in a dorsal and ventral layer, though some occur l^etween. The primordium of the Wolffian duct occurs in the angle between the somatic mesoblast and the intermediate cell-mass, and the aorta lies in the corresponding angle of the splanchnic mesoblast. In the last somite (Fig. 107) one finds two important changes: (1) the intermediate cell-mass is much broader owing to multiplication of its cells, and as a consequence the two-layered arrangement is lost; (2) whereas the cells of the intermediate cell-mass in the region of the segmental plate could not be delimited accurately from either the segmental or lateral plate, it is now easy in most sections to mark its boundary on both sides. It now constitutes, therefore^ a rather well-defined but unorganized mass of cells between the somite and lateral plate, aorta and Wolffian duct; the posterior cardinal vein appears above the Wolffian duct.

The next change, found to begin in about the twenty-sixth somite, is a condensation of a portion of the cell-mass lying median to and below the Wolffian duct (Fig. 108), rendered evident by the deeper stain in this region; the condensed portion of the original intermediate cell-mass is not, however, sharply separated from the remainder, but shades gradually into it both dorsally and ventrally, so that it can be seen to represent approximately the central part of the original middle plate. In view of its prospective function it may be called the nephrogenous tissue. Following it yet farther forward one finds that it is a continuous cord of cells with alternating denser and less dense portions, until in the twentieth somite (Fig. 109), the denser portions become discrete balls of radially arranged cells. In the eighteenth and seventeenth somites (Fig. 110) these become small thick-walled vesicles, which are situated median and ventral to the duct. Each vesicle is the primordium of a complete mesonephric tubule. Farther developed tubules are found in the fifteenth and sixteenth somites, and it is probable that the nephrogenous tissue forms mesonephric tubules in the fourteenth, thirteenth, and perhaps yet more anterior segments.

The formation of the tubules proper from the vesicles may be studied satisfactorily in a 35 s embryo (seventy-two hours). In the twenty-third somite of such an embryo the nephrogenous tissue and the nascent tubules lie median to the Wolffian duct and below the median margin of the cardinal vein (Fig. 111). The Wolffian duct is triangular in cross-section w^ith its longest and thinnest side next the coelome. The most advanced vesicle in this region possesses a hollow sprout extending laterally to the Wolffian duct with which it is in close contact; this is the primordium of the tubular part of the mesonephric tubule (cf. Fig. 114 A and B). In more anterior somites it is found that such sprouts have fused with the wall of the duct in such a manner that the lumen of the tubule now communicates with that of the duct.

Simultaneously the median portion of the original vesicle has been transformed into a small Malpighian corpuscle in the following manner: it has first become flattened so that the lumen is reduced to a narrow slit; then this double-layered disc becomes concave with the shallow cavity directed posteriorly and dorsally; at the same time the convex wall becomes thin, and the concave thick. The entire tubule thus becomes S-shaped. Figs. 114 A, B, C, D illustrate the corresponding processes in the duck, which are similar in all essential respects to the chick.

Fig. 114. — From a transverse series through a duck embryo of 45 s, to show the formation of the mesonephric tubules. (After Schreiner.) Fig. 218 shows the position of the sections A, B, and C. V. c. p., Posterior cardinal vein. W. D., Wolffian duct. A. and B. represent tubules of the twenty-ninth segment. C. of the twenty-seventh segment. D. of the twenty-fourth segment.

In the chick embryo of 35 somites the only differentiated tubules are in front of the twentieth somite, a region of the mesonephros that never develops far, and such tubules do not appear ever to become functional. In the region of the subsequent functional mesonephros (twentieth to thirtieth somites) the development has not progressed beyond the stage of the vesicles showing the first indications of budding.

The main part of the mesonephros is thus between the twentieth and thirtieth somites. In the anterior half of this region three or four rudiments of tubules are formed in each somite by the seventy-second hour. Subsequently five or six tubules are formed in each segment between the twentieth and thirtieth. Tubules are formed first from the ventral portions of the nephrogenous tissue (see Fig. Ill); those formed later arise from the unused portions. There is no evidence that they ever arise in any other way. The tubules may thus be divided according to the time of origin into primary, secondary and tertiary sets, but there is no morphological or functional distinction between the successive sets. (See Chap. XII.)

The collection of tubules causes a projection or fold on each side of the mesentery into the body-cavity, known as the Wolffian body, the detailed history of which is given in Chapter XII.

In conclusion it should be noted that the most anterior tubules of the Wolffian body possess peritoneal funnels like the pronejDhric tubules. Thus in an embryo of 30 somites I have noticed open peritoneal funnels in the eighth, ninth, twelfth, thirteenth, fourteenth, fifteenth, sixteenth, and seventeenth somites. It seems quite certain that the last of these belong to the mesonephros, though the most anterior are undoubtedly pronephric rudiments. In the eighteenth, nineteenth, twentieth, and twenty-first somites, small depressions of the peritoneum were noticed opposite tubules, but not communicating with them.

The Vascular System

Soon after the thirty-third hour the heart begins to twitch at irregular intervals, and by the fortyfourth hour its beatings have become regular and continue uninterruptedly. The contraction proceeds in the form of a rapid peristaltic wave from the posterior to the anterior end of the cardiac tube, and the blood, already present, is forced out in front. Through the aortic arches it reaches the dorsal aorta which distributes part to the body of the embryo, but most of the blood enters the vascular netv/ork of the yolk-sac. It is returned to the heart by various veins in the yolk-sac and embryo, and recommences the circuit.

The development of the vascular system will be more readily understood if we preface the account with a brief description of the anatomy of the system early in the fourth day (Fig. 115, cf. also Figs. 135 and 136).

The heart consists of four chambers, viz., the sinus venosus, the atrium the ventricular loop, and the bulbus arteriosus (Fig. 116).

The truncus arteriosus lies in the floor of the pharynx and gives off the following vessels: (1) a short branch, the external carotid, extending into the mandibular arch; (2) complete arches in the second, third, and fourth visceral arches which join the dorsal aorta; these are known as the second, third, and fourth aortic arches; the third arch is the largest.

Fig. 115. — The circulation in the embryo and yolk-sac between the eightieth and ninetieth hours of incubation, drawn from a photograph by A. H. Cole. The arteries are represented in solid black; the veins in neutral tint. A fold of the yolk-sac covers the fore part of the head, a. a. 2, .3, 4, Second, third, and fourth aortic arches. Ao., Aorta. Atr., Atrium. B. a., Bulbus arteriosus. Car. ext., External carotid. Car. int., Internal carotid. D. C, Duct 'of Cuvier. D. V., Ductus venosus. J., Jugular vein (anterior cardinal). 1. a. V., Left anterior vitelHne vein. p. V., Posterior vitelHne vein. S. V., Sinus venosus. V. c. p.. Posterior cardinal vein. Ven., Ventricle. V. O. M. L., Left omphalomesenteric vein.

The original mandibular aortic arches unite with the anterior ends of the dorsal aortse, forming a loop on each side at the base of the forebrain (Fig. 93), and they have, therefore, a different relation from the other aortic arches; it seems probable also that they have a different morphological value. The ventral limb of this loop disappears in its pre-oral part after this stage and a new vessel is formed entirely within the mandibular arch, bearing the same relation to the visceral arch as the other aortic arches. At the stage of 35 somites it is a complete arch, in some embryos at least (Fig. 117), though of very small caliber and very transitory, possibly sporadic, in its occurrence. It is possible that this is the true mandibular arch, and the pre-oral portion of the original mandibular arch should have another interpretation. Kastschenko suggests that it may have been related to lost pre-mandibular gillclefts.

The roots of the dorsal aorta above the pharynx receive the aortic arches and are continued forward as the internal carotid arteries, branching in the fore part of the head. Posteriorly the right and left aortic roots unite just behind the fourth visceral pouch to form the dorsal aorta, and this continues as an undivided vessel to about the level of the twenty-second somite, where it divides into right and left dorsal aortse, and at the same time sends out a large omphalomesenteric artery into the yolk-sac on each side, and these branch as shown in Figure 115 into the capillary network of the yolk-sac. The dorsal aortse, now much diminished in size, continue back into the tail where they are known as the caudal arteries. The dorsal aorta also sends off a pair of segmental arteries into each intersomitic septum, and a pair of small allantoic (umbilical) arteries into the primordium of the allantois.

The veins enter the heart through three main trunks: (1) the ductus venosus, (2 and 3) the paired ducts of Cuvier. These are made up as follows: (1) the ductus venosus is formed at the level of the posterior liver diverticulum by the right and left omphalomesenteric veins, which arise in the yolk-sac by union of the capillaries of the vascular area; the right vitelline vein also receives two veins coming directly from the anterior and posterior ends respectively of the sinus terminalis, the anterior of these is frequently partly double owing to its mode of origin. (See beyond. Chap. VII.) The vascular area in the yolk-sac thus appears strikingly bilateral at this time. (2 and 3) The ducts of Ciivier are made up by the union of all the somatic veins. Each is formed primarily by the union of the anterior and posterior cardinal veins. The anterior cardinal vein receives all the blood of the head, and thus includes the first three segmental veins. It also receives at its point of junction with the posterior cardinal vein a branch from the floor of the pharynx, the external jugular vein. The posterior cardinal vein receives (1) all the segmental veins of the trunk, of which there are twenty-nine pairs, running in the intersomitic septa between the fourth and thirty-third somites, and the veins of the Wolffian body of which there are several to each somite concerned, as described in the account of that organ.

The development of the vascular system up to the stage just described will now be taken up.

Development of the Heart

(a) Changes in the External Form. In the last chapter we traced the origin of the heart up to the time when it is a practically straight, undivided, somewhat spindle-shaped tube lying below the floor of the pharynx, to which it is attached by its dorsal mesentery (mesocardium). Posteriorly its cavity divides into the omphalomesenteric veins which run in the side-walls of the anterior intestinal portal. The heart is lengthened backwards by the concrescence of the omphalomesenteric veins and the most posterior division of the heart (the sinus venosus) is established in this way between the stages of 12 and 18 somites; it is marked by a broad fusion with the somatopleure (mesocardia lateralia) through which the ducts of Cuvier enter the heart.

At the stage of sixteen somites the duct of Cuvier lies opposite the hind end of the second somite on the right side, and a little farther back on the left side; and the somato-cardiac fusion (mesocardium laterale) in which it lies is of the width of about one and a half somites. On the right side the duct of Cuvier lies a little in front of, and on the left side a little behind, the point of union of the omphalomesenteric veins; thus the posterior end of the heart is not fully formed at the stage of 16 s, but is at the stage of 18 s. The subsequent fusion of the omphalomesenteric veins produces the so-called ductus venosus, or main splanchnic vein, which is therefore a posterior continuation of the sinus venosus.

The cardiac tube proper lies between the origin of the aortic arches at the anterior end and a point a Uttle behind the entrance of the ducts of Cuvier into the heart at the posterior end.

Two main changes characterize the development of the heart in the period under consideration: (1) folding of the cardiac tube and (2) differentiation of its walls in successive regions to form the four primary chambers of the heart, viz. (from behind forwards), the sinus venosus, the auricular division (atrium), the ventricular division and the bulbus arteriosus.

The folding of the heart is caused by the rapid growth between its anterior and posterior fixed ends, and the places of folding are determined largely by differences in the structure of the walls at various places. The folding begins by a curvature to the right, and this proceeds until the tube has an approximately semicircular curvature (Fig. 72). At a certain place in the curved tube a very pronounced posterior projection takes place (Figs. 73 and 74), and at the same time this bent portion turns ventrally; the apex of the bend represents the future apex of the ventricles. The continuation of these two directions of folding then brings the ventricular division of the heart immediately beneath the sinu-auricular division which is attached dorsally by the somato-cardiac connections; further continuation brings the apex of the heart a little behind the auricular portion (Figs. 85, 87, 88, 93, 99). During all this period the distance between the two fixed ends has remained practically constant.

During the process of folding, constrictions have arisen between successive portions of the cardiac tube, owing to expansion of intervening portions, and thus at the stage of seventy-two hours the heart shows the following divisions and form. From the dorsal surface (in a dissection, Fig. 116) one sees (1) the sinus venosus, broad behind and narrow in front where it joins the auricular division; it receives three veins: (a) the large ductus venosus, appearing as a direct posterior continuation of the sinus, and separated from it by only a slight constriction; and (6 and c) the right and left ducts of Cuvier entering the sinus laterally and dorsally near its enlarged posterior end; (2) the sinus enters the atrium through the dorsal wall; the atrium shows two lateral expansions, the future auricles, of which the left is much the more expanded at this time; the sinus appears partly sunk in the right auricle. (3) Only the right limb of the ventricular loop is visible from the dorsal surface at this time, and is separated from (4) the bulbus arteriosus by a slight constriction. The biilbus thus Hes on the right side; it sweeps around the atrium anteriorly to the middle line and then bends up to enter the floor of the pharynx.

From the ventral side one sees the looped ventricular division behind, in which we distinguish right and left limbs, the former of which enters the bulbus in front, and the latter the auricles. These two limbs represent approximately the future right and left ventricles (Fig. 198, Chap. XII).

In an ordinary entire mount of this stage the heart is seen from the right side, and the disposition of the parts may be readily understood by reference to Fig. 117, and the preceding description.

Another change that should be noted here is the disappearance of the mesocardium during the folding of the cardiac tube, except in the region of the sinus venosus where it remains permanently and becomes much broadened (seventy-two hours).

(6) Changes in the Internal Structure of the Heart. We have already seen that the heart consists of two primary layers, viz., the endocardium, which is endothelial in nature, and the myocardium, which is derived from the splanchnic mesoblast. The distinction between the sinu-auricular and the bulbo-ventricular divisions of the heart is indicated internally at about the time the first external evidence is seen, by the fact that the endocardium is more closely applied to the myocardium in the former than in the latter division. In the sinus and atrium but little change takes place in the period under consideration. In the ventricle, on the other hand, and especially in the right limb, the wide space originally existing between endocardium and myocardium becomes more or less filled by multiplication of the endocardial cells. On the side of the myocardium there is first a thickening, and then anastomosing processes are sent out towards the endocardium. Cavities also arise within the thickened myocardium and all communicate. The endocardial cells then form a covering to all myocardial processes and cavities, and the cavities thus lined communicate with the main endocardial cavity. Thus the wall of the ventricles becomes spongy and all the cavities in it are lined by a layer of endocardium and communicate with the endocardial cavity. In the bulbus finally there is a great thickening of the endocardium produced by multiplication of its cells, but no corresponcUng change in the myocardium; thus the bulbus at seventy-two hours shows a thin myocardial and a thick endocardial wall. The later development is described in Chapter XII.

Fig. 116 . — Heart of a chick embryo of 72 hours, dissected out and drawn from the dorsal surface.

Aur. 1., Left auricle. Aur. r., Right auricle. B. a., Bulbus arteriosus. D. C. r. 1., Right and left ducts of Cuvier. D.V., Ductus venosus. S.V., Sinus venosus. Tr. a., Truncus arteriosus. V. r., Right limb of ventricle.

The Arterial System

The description of the development of the arterial system proceeds from the stage of 12 somites described in the last chapter.

The primitive vascular system of vertebrate embryos is a capillary netw^ork in all parts of the blastoderm and of the embryo. Main trunks arise by development of parts of the network corresponding to the rate and direction of embryonic growth and thus answering to the vascular needs of growth. The vascular system forms at all stages a continuous endothelial tree whose primitive form in all parts is a capillary network. This idea, which we owe originally to Aeby, has been worked out in a masterly way by H. M. Evans. (See lit. Chap. V.)

The Aortic Arches

An arch of the aorta is formed in each visceral arch; they arise successively as buds from the roots of the dorsal aorta in the order and time of formation of the visceral arches. Thus the first or mandibular aortic arch is formed at the stage of 9-10 somites; the second or hyoicl aortic arch arises from the dorsal aorta at about the stage of 19 s and joins the ventral aorta at about the 24 s stage. The third is completely formed at the stage of 26 somites. The fourth is completely formed at the stage of 36 somites; and the fifth and sixth arise during the fourth and fifth days. (See Chap. XII for account of the fifth and sixth arches.)

The first aortic arch loses its connection with the dorsal aorta at about the stage of 30 somites, and the second arch similarly during the fourth clay; the ventral ends of these arches retain their connection with the ventral aorta and constitute the beginning of the external carotid. Thus the third, fourth, fifth and sixth aortic arches remain. Their transformation belongs to the subject-matter of Chapter XII.

The pulmonary artery appears as a posterior prolongation of the ventral aorta on each side at about the 35 s stage. It thus appears successively in later stages as a branch from the base of the fourth and sixth aortic arches.

The Internal Carotids

The loop where the mandibular arch joins the dorsal aorta may be called the carotid loop; it is situated in front of the oral plate at the base of the fore-brain on each side (Fig. 93). It enlarges to form a sac, and when the connection with the mandibular arch is lost, sends out branches into the tissue surrounding the brain. These are of course a direct continuation of the dorsal aorta on each side.

The segmental arteries are paired branches of the dorsal aorta in each intersomitic septum. They pass dorsally to about the center of the neural tube and arch over laterally to enter the segmental veins, and thus unite with the cardinal veins.

The Development of the Venous System

The main outlines of the development of the venous system have been already considered.

The somatic veins, i.e., the anterior and posterior cardinal veins and their branches, enter the sinus venosus through the ducts of Cuvier. The original position of this duct as we have seen is about the level of the second somite. The formation of the cervical flexure, however, carries a number of somites forward above the heart, so that at about the stage of 32 s it comes to lie in the region of the eighth and ninth somites. The relation betw^een the somatopleure and the heart in this region has been already described.

The anterior cardinal veins are the great blood-vessels of the head, and become the internal jugulars in the course of development. Owing to the order of development of the body, the anterior cardinals are formed before the posterior cardinals. At the 15-16 s stage they lie at the base of the brain, dorsal and lateral to the dorsal aortse, and extend forward to the region of the diencephalon. They he internal to the cranial nerves and pass just beneath the auditory pits.

As the brain develops many branches of the anterior cardinal veins arise, the most conspicuous of which at seventy-two hours are a large branch just behind the auditory sac, one between the auditory sac and the trigeminal ganglion, an ophthalmic branch extending along the base of the brain to the region of the optic stalks and a network of vessels on the lateral surfaces of the fore-brain. The other branches of the anterior cardinal vein are the three anterior intersomitic veins (Fig. 115); the external jugular from the floor of the pharynx enters the duct of- Cuvier just beyond the union of the anterior and posterior cardinal veins.

Up to about forty-eight hours the anterior cardinal veins lie median to the cranial nerves, but between this time and seventytwo hours the facial and glossopharyngeal nerves cut completely through the vessel and thus come to lie median to it; the trigeminus and vagus continue to lie lateral to it.

The posterior cardinal arises as a posterior prolongation from the duct of Cuvier and grows backward above the Wolffian duct, keeping pace with the differentiation of the intermediate cellmass, as far as the thirtv-third somite. It does not enter the caudal region of the body. As already described it receives twenty-nine intersomitic veins and the veins of the Wolffian bodv. At first its connection with the duct of Cuvier is by means of a network of vessels, which gradually gives place to a single trunk (cf. Fig. 117).

The Splanchnic Veins

The ductus venosus is the unpaired vein immediately behind the sinus venosus, formed by fusion of the two omphalomesenteric veins. It is fully formed at the stage of 27 somites. Its relations to the liver have already been described in connection with that organ. Its subsequent changes are described in Chapter XII.

The vitelline veins are united at about the stage of seventytwo hours by a loop passing over the intestine immediately behind the pancreas. (See Chap. XII.)

VII. The Body-cavity and Mesenteries

The origin of the dorsal and ventral mesenteries was considered in the section of this chapter dealing with the alimentarv canal. As noted there, the dorsal mesentery extends the entire length of the ahmentaiy canal, while the ventral mesentery persists only in the region of the fore-gut and the cloaca.

Fig. 117. — Entire embryo of 35 s, drawn as a transparent object. a. a. 1, 2, 3, 4, First, second, third, and fourth aortic arches. Ar., Artery. A. V., ViteUine artery, cerv. FL, Cervical flexure, cr. Fl., Cranial flexure. D. C, Duct of Cuvier. D. V., Ductus venosus. Ep., Epiphysis. Gn. V., Gantrlion of trigeminus. Isth., Isthmus. Jug. ex.. External jugular vein. Md., Mandibular arch. M. M., Maxillo-mandibular branch of the trigeminus, olf. P., Olfactory pit. Ophth., Ophthalmic branch of the trigeminus. Ot., otocyst. V., vein. W. B., Wing bud. V. c. p., Posterior cardinal vein. V. umb.. Umbilical vein. V. V., Vitelline vein. V. V. p., Posterior vitelline vein.

The embryonic body-cavity shows two divisions from a Yery early stage, viz., (1) the large cephalic or parietal cavity situated in the pharyngeal region of the head and containing the heart, and (2) the general pleuroperitoneal cavity of the trunk. After the heart is established in the middle line the parietal cavity is bounded posteriorly by the wall of the anterior intestinal portal (Figs. 75, 85, etc.), but it communicates with the pleuroperitoneal cavity around the sides of the portal, in which the vitelline veins run. Laterally the parietal cavity communicates with the extra-embryonic body-cavity.

The mesocardia lateralia are also an important landmark in the embryonic body-cavity because from them proceed the partitions that subsequently separate the pericardial and pleural cavities on the one hand, and the pleural and peritoneal bodycavities on the other. (See Chap. XI.) The primordium of the lateral mesocardia may be recognized in the 10 s stage : just behind the heart the median portion of the body-cavity is thick-walled, the peritoneal cells being actually columnar. At this place, a short distance lateral to the median angle of the body-cavity, and at the junction of the cylindrical and flat mesothelium, a fusion of considerable longitudinal extent is formed between the somatopleure and the proximal portion of the vitelline veins, projecting up from the splanchnopleure; this fusion is the beginning of the lateral mesocardiam. It separates a more median portion of the body-cavity from a more lateral, and in it the duct of Cuvier soon develops.

When this portion of the body of the embryo becomes elevated (forty to fifty hours) the portion of the body-cavity lateral to the mesocardia lateralia comes to lie ventrally to the median portion (cf. Fig. 69), and at the same time the lateral mesocardia rotate around a longitudinal axis through an angle of about 90°, so that the original median border becomes dorsal, and the original lateral border becomes ventral. The dorsal divisions, right and left, of the pleuroperitoneal cavity may now be called the pleural grooves. Inasmuch as the parietal cavit}^ has receded considerably at the same time into the trunk with the elongation of the fore-gut, it comes to lie beneath the pleural grooves instead of in front of them as before. Therefore in cross-sections, in front of the lateral mesocardia, the pleural grooves appear as dorsal projections of the parietal (later pericardial) cavity, separated from one another in the middle line by the oesophagus (Fig. 118).

The relations of the three divisions of the embryonic bodycavity thus established may be described as follows: the parietal cavity contains the heart, and is therefore the prospective peri

Fig. 118. — Transverse section of an embryo of 35 s, immediately in front of the lateral mesocardia. Ao., Aorta. Atr., Atrium. B. a., Bulbiis arteriosus. D.C. r , and'l., Ri^ht and left ducts of Cuvier. Lg., Lung, m's'c. dors., Dorsal' mesocardium. m's't. dors., Dorsal mesentery. P. C, Pericardial cavity, pi. gr., Pleural groove. Rec. pul. ent., Recessus pulmo-entericus. S. V., Sinus venosus.

cardial cavity. It is not, however, a closed cavity, but communicates in front of the lateral mesocardia with the pleural grooves (Fig. 118), and by way of the latter above the lateral mesocardia with the peritoneal cavity (Figs. 119 and 120); a second communication of the parietal cavity with the peritoneal cavity is beneath the lateral mesocardia around the sides of the anterior intestinal portal, now being converted into the septum transversum (cf. Fig. 120). A more complete description of the cavities is given in Book - The development of the chick (1919) 11Chapter XI]].

The median wall of the pleural grooves forms much mesoblast during the formation of the lung diverticula, and thus initiates the formation of lobes enclosing the lungs (Figs. 118 and 119). These lobes descend ventrally and unite with the septum transversum (see below), thus producing blind bays of the coelome at the sides of the oesophagus, known as the superior recesses of the peritoneal cavity or pulmo-enteric recesses.

Fig. 119. — Transverse section of the same embryo through the lateral mesocardia.

Liv., Liver, m's'c. lat., Lateral mesocardium. m's't. access Accessory mesentery, m's't. ven., Ventral mesentery. Other abbreviations as before.

The ventral mesentery extends from the anterior end of the sinus venosus to the hind end of the fore-gut, where it unites with the ventral body-wall. It includes the sinus venosus and the ductus venosus, together with the hepatic diverticula. The median and lateral mesocardia, together with the ventral mesentery of the fore-gut, form a mass known as the septum transversum.

At the stage of seventy-two hours, then, the pleural, pericardial and peritoneal divisions of the body-cavity are indicated, but all are in communication. The pleural cavities connect with the peritoneal cavity posteriorly, and with the pericardial cavity anteriorly in front of the lateral mesocardia (Figs. 118, 119, 120); and the pericardial cavity communicates also with the peritoneal cavity beneath the lateral mesocardia around the roots of the vitelline veins (sides of the anterior intestinal portal). Thus the ducts of Cuvier and the vitelline veins are the agencies that introduce the separation of the body-cavities.

Fig. 120. — Transverse section of the same embryo immediately behind the lateral mesocardia. ant. hep. Div., Anterior hepatic diverticulum. Duod., Duodenum. End'c, Endocardium. D. V., Ductus venosus. My'c, Myocardium. PI. m's'^., PHca mesogastrica. S-am., Sero-amniotic connection, ven. r., 1., Right and left limbs of the ventricle. V. umb., Umbilical vein.

The tail-fold forms blind coelomic pockets in the region of the hind-gut, which end in the region of the thirty-third somite. (Of. Fig. 81.)

Lillie 1919: Introduction | Part 1 - 1 The Egg | 2 Development Prior to Laying | 3 Outline of development, orientation, chronology | 4 From Laying to Formation of first somite | 5 Head-fold to twelve somites | 6 From twelve to thirty-six somites | Part 2 - 7 External form of embryo and embryonic membranes | 8 Nervous system | 9 Organs of special sense | 10 Alimentary tract and appendages | 11 The body-cavities, mesenteries and septum transversum | 12 Later development of the vascular system | 13 Urinogenital system | 14 Skeleton | Appendix | Frank Lillie

Cite this page: Hill, M.A. (2024, April 17) Embryology Book - The development of the chick (1919) 6. Retrieved from

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