Book - The development of the chick (1919) 12

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

Part II The Forth Day to Hatching, Organogeny, Development of the Organs

CHAPTER XII THE LATER DEVELOPMENT OF THE VASCULAR SYSTEM[edit] I. The Heart. (For an account of the earlier development,

see Chapters V and VI.)

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

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

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

199 and 200).

The auricles arise as lateral expansions of the atrium, the

348

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

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

LATER DEVELOPMENT OF VASCULAR SYSTEM

349

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

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

chick embryo of 5 mm. head-length.

(After Masius.)

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

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

350

THE DEVELOPMENT OF THE CHICK

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

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

Masius.)

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

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

LATER DEVELOPMENT OF VASCULAR SYSTE:\r 351

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

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

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

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

352

THE DEVELOPMENT OF THE CHICK

,

. AS. So p.

/

/^

(^S)

1

w

A.Sao.p.

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

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

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

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

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

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

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

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

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

LATER DEVELOPMENT OF VASCULAR SYSTEM 353

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

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

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

354

THE DEVELOPMENT OF THE CHICK

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

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

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

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

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

LATER DEVELOPMENT OF VASCULAR SYSTEM

355

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

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

(e) Completion of the Septa.

Fig. 203. — Reconstruction of the

heart of a chick embryo of 5.7 mm.

head-length, seen from right side.

Part of the wall of the right auricle

is cut away. (After Masius.)

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

Thus bv the end of the fifth

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

356

THE DEVELOPMENT OF THE CHICK

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

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

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

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

LATER DEVELOPMENT OF VASCULAR SYSTEM 357

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

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

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

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

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

358 THE DEVELOPMENT OF THE CHICK

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

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

II. The Arterial System

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

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

LATER DEVELOPMENT OF VASCULAR SYSTEM

359

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

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

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

Fig. 205. — Diagram of

the aortic arches of birds

and their fate. (After

Boas.)

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

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

360 THE DEVELOPMENT OF THE CHICK

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

on both sides of the body.

During the fifth and sixth

days the two sides become

asymmetrical, the fourth arch

becoming reduced on the left

side of the body and enlarged

on the right. Fig. 207 shows

the condition on the two sides

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

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

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

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

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

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

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

A. Left side.

B. Right side.

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

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

LATER DEVEL0P:\IEXT OF VASCULAR SYSTEM 361

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

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

<^M

A B.

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

A. Left side.

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

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

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

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

362

THE DEVELOPMENT OF THE CHICK

Car. cow

s.cl.s

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

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

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

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

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

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

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

with its branches (Fig. 216).

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

LATER DEVELOPMENT OF VASCULAR SYSTEM 363

a longitudinal anastomosis communicating with the internal carotid in front.

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

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

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

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

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

first venous trunks)

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

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

364 THE DEVELOPMENT OF THE CHICK

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

the sinus venosus.

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

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

LATER DEVELOPMENT OF VASCULAR SYSTEM

365

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

M^

//it.

' ■ \ Af.y.

A

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

A. About the fifty-eighth hour.

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

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

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

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

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

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

366 THE DEVELOPMENT OF THE CHICK

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

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

meatus venosus.

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

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

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

LATER DEVELOPMEXT OF VASCULAR SYSTEM ' 367

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

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

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

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

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

368 THE DEVELOPMENT OF THE CHICK

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

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

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

LATER DEVELOPMENT OF VASCULAR SYSTEM

369

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

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

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

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V.u.d

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

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

the veins in the region of the liver of a sparrow

embryo. Outline of the liver represented by

broken lines. Dorsal view. (After Miller.)

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

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

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

Right and left umbilical veins.

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

The venous circulation is then as follows: The blood from

370

THE DEVELOPMENT OF THE CHICK

Ucp.d.

A-o.m.

Vsc.d.

LATER DEVELOPMENT OF VASCULAR SYSTEM 371

C. V.sc.d.

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V.c.i.

A.OM

V.c.fi.d.

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

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

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

372 THE DEVELOPMENT OF THE CHICK

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

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

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

IV. The Embryonic Circulation

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

The blood is returned to the heart through the sinus venosus

LATER DEVELOPMENT OF VASCULAR SYSTEM 373

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

d., s.

c. i. SC,

V. V. g.,

V. i. i.,

Right and left vena intervertebralis lum

Vena iliaca interna. V. i. 1.

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

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

374

THE DEVELOPMENT OF THE CHICK

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

sinus venosus, viz., that re

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

-- Vils.

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

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

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

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

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

LATER DE\ ELOPMEXT OF VASCULAR SYSTEM 375

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

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

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

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

376 THE DEVELOPMENT OF THE CHICK

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

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

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

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

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

on the sixth day of incubation.

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

LATER DEVELOPMENT OF VASCULAR SYSTEM 377

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