Vertebrate Embryology - A Text-book for Students and Practitioners (1893) 5

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A personal message from Dr Mark Hill (May 2020)  
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I have decided to take early retirement in September 2020. During the many years online I have received wonderful feedback from many readers, researchers and students interested in human embryology. I especially thank my research collaborators and contributors to the site. The good news is Embryology will remain online and I will continue my association with UNSW Australia. I look forward to updating and including the many exciting new discoveries in Embryology!

Marshall AM. Vertebrate Embryology: A Text-book for Students and Practitioners. (1893) Elder Smith & Co., London.

Marshall (1893): 1 Introduction | 2 Amphioxus | 3 Frog | 4 Chick | 5 The Rabbit | 6 Human Embryo | Illustrations
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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Contents

Chapter V. The Development of the Rabbit

Preliminary Account

The rabbit may conveniently be taken as a typical member of the Mammalia, the highest group of Vertebrates.

Mammals differ notably from the animals dealt with in the previous chapter in being viviparous ; that is. in bringing forth their young alive, instead of laying eggs. This difference, .though at first sight a striking one, is really of but secondary importance ; and the actual processes of development of the Mammal are effected in the same way as in the oviparous Vertebrates.

Amphioxus and the frog lay their eggs in water, and the eggs are not even fertilised until they have left the body of the mother. In the Bird the eggs are fertilised as they leave the ovary and enter the oviduct, and the earliest stages of development are effected during the passage of the egg down the oviduct ; the egg at the time of laying having already been developing for eighteen hours or more. However, although development, in the case of the bird, commences while the egg is still within the parent, it is only the earliest phases segmentation of the egg and the establishment of the germinal layers that are effected in this position ; the formation and development of the embryo itself not commencing until after the egg has been laid.

In the Mammal, on the other hand, the ovum is retained within the oviduct and uterus of the mother for a very much longer time ; and the whole embryonic development is completed before leaving the parent ; the young Mammal at the time of birth being fully formed, and of considerable size, though not yet fit for independent existence.

The rabbit embryo, like that of other animals, is developed from an ovum or egg, which, as in other animals, is a single nucleated cell, of epithelial origin. This ovum, after being fertilised by a spermatozoon from the male, undergoes cell division or segmentation, which, as in the bird, is effected during the passage of the ovum along the oviduct. On reaching the uterus, which is simply the distal, enlarged end of the oviduct, the ovum halts, becomes fixed to the wall of the uterus, and there remains during all the further stages of development, up to the time of birth.

The actual details of development of the rabbit embryo, the mode of formation of its various organs, and even the proportions of the several parts and the order of their appearance, are essentially the same as in the chick. The most noteworthy point of difference is the exceeding slowness with which the earlier stages are passed through in the rabbit.

The entire period of development of the rabbit, from the discharge of the ovum from the ovary, to the birth of the young animal, occupies thirty days. Of this time the first three days are spent by the egg in passing down the oviduct, and in undergoing segmentation ; and it is not until the seventh day that the first trace of the embryo appears ; the rabbit's ovum at the end of the seventh day being in a condition closely corresponding to that of the chick about the end of the first day of incubation (cf. Figs. 107 and 143). From this time, development proceeds much more rapidly, at about the same rate as in the chick, a twelve-day rabbit embryo (Fig. 161) corresponding closely in structure, and in actual size, with a five-day chick embryo (Fig. 115).

The eggs of the three animals described in the previous chapters differ very greatly in size. That of Amphioxus has a diameter of only O'l mm. ; the frog's egg measures about 1'75 mm. ; and the yolk, or true ovum, of the hen's egg about 30 mm. ; i.e. in round numbers the frog's egg is 5,000 times, and the hen's egg 27,000,000 times the bulk of that of Amphioxus. It has been already shown that the dimensions of the egg are chiefly governed by the amount of food-yolk which it contains, and that the size of the young animal on leaving the egg is directly dependent on the amount of this food material ; the tadpole on hatching being far larger than the Amphioxus larva, while the chick on leaving the egg vastly exceeds the tadpole in bulk.


From the large size of the young rabbit at birth it might be inferred that the rabbit's ova or eggs were large. This, however, is not the case ; the egg of the rabbit is really very small indeed, and, at the time it leaves the ovary, measures only O116 mm. in diameter, i.e. is practically the same size as the egg of Amphioxus, and only a fifteenth the diameter of the frog's egg.

It is clear that this very small egg could not develop into an animal the size of a rabbit at birth unless it received a very plentiful supply of nutriment from without ; and inasmuch as the whole increase in bulk takes place while the embryo is within the uterus, it follows that there must be some arrangement in the uterus for supplying it with food.

This is effected by means of a special organ known as the placenta, in which blood-vessels, derived from the embryo and from the mother respectively, lie side by side in very close and extensive contact with one another. The two sets of blood-vessels, foetal and maternal, are distinct, but interchange of fluid and gaseous contents takes place readily, by diffusion through their thin walls, and in this way the blood of the embryo receives nutrient matter from the blood of the mother during the whole period of gestation.

The placenta is formed practically by the allantois, which develops as an outgrowth from the alimentary canal of the embryo, and which at an early period becomes closely attached to the wall of the uterus of the mother. The blood-vessels of the allantois are, as in the chick, directly continuous with those of the embryo; and, by the outgrowth of vascular processes of the allantois into the walls of the uterus, the vessels of the embryo are brought into intimate relation with the large, dilated, and very thin-walled blood-vessels of the uterus itself.

Although the eggs of the rabbit, like those of nearly all other Mammals, are very small indeed, yet in the mode of their development they agree in several respects with the large eggs of the bird, rather than with the smaller ones of the frog, or of Arnphioxus. A large yolk-sac, for instance, is formed from the rabbit's ovum, although it contains no food material whatever ; the embryo appears in the middle of the blastoderm, and there is a well-marked primitive streak present ; while the formation of the amnion and allantois are further points of resemblance with the chick, and of difference from the frog or Amphioxus.


These and other features in the development of Mammals, which will be described more fully later on in this chapter, are best explained by supposing that existing Mammals are descended from forms in which a greater amount of yolk was present, and in which the eggs were consequently of larger size ; and that, in accordance with the Recapitulation Theory, existing Mammals have consequently an inherited tendency to develop after the manner of forms with large eggs. The lowest group of Mammals now living, the Monotremes of the Australian region, afford strong evidence of the truth of this view, as, unlike other Mammals, they are oviparous, laying eggs about the size of olives, and closely resembling the eggs of many Reptiles.

The young rabbit at birth has not yet completed its development. Its eyes are closed, like a kitten's ; and it is quite incapable of obtaining food for itself, being dependent for a time on the supply of milk afforded it by the mammary glands of the mother. Using the word gestation for the whole period of development, from the first appearance of the embryo to the time when the young animal becomes capable of independent existence, two stages may be distinguished in it : (i) uterine or placental gestation, which comprises the period prior to birth, during which the embryo is nourished by osmotic interchanges between its blood and that of the mother ; and (ii) mammary gestation, which embraces the period after birth, during which the young animal is nourished by the milk yielded by the mother.

The relative lengths of these two periods vary greatly in different Mammals. In the Marsupials, a lowly organised group, the uterine gestation is very short, the young animal, as in the kangaroo or opossum, being born at an early stage, of small size, and very imperfectly developed ; while in the higher Mammals the period of uterine gestation is a much longer one, and the young animals at birth are of larger size, and more completely formed.

The Egg

1. Formation of the Egg

To study the mode of formation of the ova in the rabbit it is necessary, as in the chick and frog, to take, not adult animals nor even new-born young, but embryos at an early stage of development.

In a rabbit embryo of about the eleventh day, a pair of ridge-like thickenings of the peritoneal epithelium appear, close to the mesentery, and along the inner sides of the Wolffian bodies. These genital ridges (Fig. 165, GR) constitute the earliest stage in the development of the ovaries, and are at first caused merely by an alteration in the shape of the epithelial cells of the peritoneum, which, elsewhere flattened, become here columnar.

The genital ridges soon become more prominent, partly through an increase in the thickness of the epithelium, which becomes two or three cells deep ; and partly through the ingrowth into each ridge of an axial core of connective tissue.

The genital ridge (Fig. 165) lies very close to the Wolffian. body ; and, about the fourteenth day, solid columns of cells grow out from the Malpighiaii bodies of the anterior end of the Wolffian body into the ridge. These columns of cells form what is called the tubuliferous tissue of the ovary ; in the early stages they occupy almost the whole of the axial part of the genital ridge, but as development proceeds they gradually become less conspicuous, and withdraw more or less completely from the ridge. They have nothing whatever to do with the formation of the ova.

In a rabbit embryo of the eighteenth day the genital ridges have grown considerably, and project into the body cavity as a pair of longitudinal folds, close to the attachment of the mesentery to the dorsal body wall. Each ridge is covered by the germinal epithelium, which consists of two or three layers of cells, the outermost of which are columnar in shape, while the more deeply placed ones are more or less spherical. The central part, or core, of the genital ridge is made up almost entirely of the tubuliferous tissue, with numerous blood-vessels and a small amount of connective tissue.

By the twenty- second day the germinal epithelium has increased considerably in thickness ; and among the cells of which it consists are some of larger size than the rest, these larger cells being the primitive ova. By the twenty-eighth day, i.e. about two days before birth, the genital ridges are still larger ; the germinal epithelium covering their surface is much thicker than before, and its deeper layers are honeycombed, or broken up into irregular columns, by ingrowth of the vascular connective tissue from below.


A thin layer of connective tissue, the tunica albuginea, extends parallel to the surface of the ovary, and divides the germinal epithelium into two almost completely separate layers ; a thin outer layer of columnar cells, investing the outer surface of the ovary ; and a much thicker, deeper layer of spherical cells, broken up into nests by the connective tissue partitions. In the germinal epithelium, and more especially in its outer layer, the primitive ova are conspicuous, as individual epithelial cells, much larger than their neighbours, and usually spherical or polygonal in shape, with large granular nuclei. The tubuliferous tissue is still present along the axis of the ovary, but now occupies a relatively much smaller space than before.

The permanent ova. Four or five days after birth of the young rabbit, the germinal epithelium undergoes further changes, marking the establishment of sexuality, and the conversion of the genital ridge of the embryo into the definite ovary.

The changes consist essentially in the formation of permanent ova from the primitive ova, and occur in the rabbit in much the same way as in the chick or tadpole. The nucleus, or germinal vesicle, increases in size and becomes vesicular, acquiring a very distinct nuclear membrane ; the nuclear contents collect to one spot, where they form a granular mass, from which, by branching, a definite reticulum is established ; and, finally, one or more of the nodal points of the reticulum enlarge, to form the nucleoli or germinal spots.

The other cells of the germinal epithelium have small nuclei } and soon arrange themselves in a more or less definite manner, so as to form follicles surrounding the permanent ova (Fig. 133, GA).

At first (Fig. 133, oz), each nest of epithelial cells may contain several permanent ova, but as development proceeds, and as the follicle cells become more definitely arranged around the ova, the nests are broken up by further ingrowth of the vascular connective tissue, and the separate follicles isolated from one another.

Although it appears to be the rule in the rabbit's ovary that each primitive ovum should become a permanent ovum, yet this is by no means always the case. Sometimes two or more primitive ova fuse together to form a bi-nuclear or poly-nuclear mass, in which all the nuclei but one may disappear, the fused mass with the remaining nucleus becoming a permanent ovum ; while in other cases it is stated that after a follicle has been formed round the fused mass, the entire mass, with the follicle, may divide into two or more permanent ova.

The development of the permanent ova proceeds from the surface of the ovary towards its deeper parts. In young rabbits, about a week after birth, the surface epithelium of the ovary contains numerous primitive ova in process of formation ; deeper down, beneath the tunica albuginea, are nests of epithelial cells in which are permanent ova in the early stages of their formation, surrounded by imperfectly formed follicles ; while still lower, in the deepest parts of the germinal epithelium, the nests are in many places broken up into isolated follicles, each containing a large and well-formed permanent ovum.


FIG. 133. Section through part of the ovary of an adult Rabbit. The section is taken vertical to the surface of the ovary, and shows one fully formed Graafian follicle, and others in various stages of development, x 50.

GrA, follicle cells surrounding an ovum. Q-B, outer layer of Graafian follicle, or ' tunica granulosa.' GrC, inner layer of Graafian follicle, or ' discus proligerus." GK, cavity of Graafian follicle. OE, outer layer of columnar epithelial cells, investing the ovary. OW, ovum. OY, primitive ovum. OZ, nests of epithelial cells derived from the deeper layers of the genital epithelium.


2. The Graafian FoUicles

Each follicle consists, at first, of a single layer of cells surrounding an ovum, the cells being derived directly from the germinal epithelium, and being therefore morphologically comparable with the ova themselves. Very shortly, each follicle becomes two-layered (Fig. 133, GA), the second layer appearing within the first one, between this and the ovum. As to the origin of this second layer of follicular cells opinions differ ; if is generally held to be formed by division of the cells of the originally single layer ; but some investigators maintain that it is derived from the ovum itself.

Immediately around the ovum, between it and the inner layer of follicle cells, a thick non-cellular layer, with faint radial striations, the zona radiata, is formed, apparently as a cuticular secretion from either the ovum or the follicle cells. Yolkgranules, elaborated by the follicle cells, accumulate within the ovum, which consequently increases in size.

The follicle cells increase rapidly by cell-division, so that the follicle soon becomes several cells thick. The outer layer of cells now grows much more rapidly than the inner layer, so that a space, somewhat crescentic in section, and filled with fluid, appears between the two layers (Fig. 133).

By further growth of the two layers, the fully-formed Graafian follicle (Fig. 133, GK) is established. This consists of, (i) an outer layer of follicular cells, GB, arranged three or four cells deep, and invested by the vascular connective tissue of the ovary ; and (ii) an inner layer of similar cells, GC, which closely invests the ovum, ow. This inner layer is attached to the inner surface of the follicle, with which it is also connected by irregular radiating strands of follicular cells, well shown in Fig. 133. The cavity of the Graafian follicle is filled with fluid.

The riper egg-follicles lie at first, as noticed above, in the deeper parts of the ovary ; but as the Graafian follicles enlarge they gradually extend nearer and nearer to the surface, and when fully formed cause rounded projections on the surface of the ovary (Fig. 133). This enlargement of the Graafian follicles, with accompanying ripening of the ova, occurs successively in different parts of the ovary, so that there are never more than a limited number, half a dozen or so, of ripe Graafian follicles at any one time in a given ovary.


Having reached its full size, the Graafian follicle ruptures at its most prominent part, and the ovum is discharged on the surface of the ovary, from which it is normally taken up at once by the fimbriated mouth of the oviduct. After discharge of the ovum, the walls of the Graafian follicle undergo a series of curious changes, which will be more fully described in the chapter dealing with the human embryo, and which result in the formation of the corpus luteum, a body which disappears early if the ovum is not fertilised ; but which, if the ovum is fertilised and develops into an embryo, persists in the ovary during the whole period of development, and is even recognisable at the time of birth of the young rabbit.

Of the two layers of the Graafian follicle, the outer (Fig. 133, GB) is sometimes spoken of as the tunica granulosa ; and the inner, GC, as the discus proligerus ; these names, however, and especially the latter one, are badly chosen, and it will be well if they drop out of use altogether.

The ovum, surrounded by the inner layer of the Graafian follicle, may be attached to any part of the outer layer of the follicle : it not uncommonly lies at the side nearest the surface of the ovary, but it may occur at the opposite or deepest part of the follicle, or at any other part of its inner surface.

The meaning of the Graafian follicle has been much debated : the most probable explanation seems to be that it is in some way associated with the great diminution in size which there is strong reason for thinking that the ovum has undergone during the evolution of the existing types of Mammals.

3. Maturation of the Egg

The nucleus of the ovum is at first centrally placed : but some time before the Graafian follicle reaches its full development, the nucleus moves towards the surface of the ovum. The exact changes that then occur have not been determined with certainty in the case of the rabbit : so far as they are known, they agree closely with those already described in the case of the frog.

A thin, homogeneous vitelline membrane is formed within the zona radiata, and apparently from the egg itself: the nucleus of the egg becomes inconspicuous ; the yolk retracts slightly from the vitelline membrane, and the first polar body is extruded from the egg.


At this stage the egg is liberated, by rupture of the Graafian follicle, and is taken up by the mouth of the oviduct. It is invested by the thin vitelline membrane, outside which is the much thicker zona radiata. More or fewer of the cells of the inner layer of the follicle usually remain adhering to the zona radiata.



FIG. 134. A fully formed ovum of a Rabbit, shortly before its discharge from

the ovary. (After Bischoff.) x 200.

FIG. 135. A Eabbit's ovum, from the upper end of the oviduct, after extrusion of the two polar bodies. (After Bischoff.) x 200.

MO, spermatozoon. N", nucleus or germinal vesicle. NTT, nucleolus or germinal spot. PB, polar bodies. Z, zona radiata.


After entering the oviduct, but before fertilisation is effected, a second polar body, apparently not more than half the size of the first one, is extruded from the egg (Fig. 135, PB).

4. Ovulation

Throughout the warmer part of the year, there is a periodically recurring ripening and discharge of ova from the ovaries of the doe rabbit. From April to July this periodic discharge, which is spoken of as ovulation, occurs regularly, and at monthly intervals : after July it usually takes place with less regularity.

The total period occupied in the development of the young rabbit, from fertilisation of the egg to the time of birth, is thirty days : that is to say, the total period of development is in the rabbit of the same length as the interval between two successive acts of ovulation.

The ovary of the doe rabbit, at the time she gives birth to young, usually contains fully formed Graafian follicles, with ripe ova ready for discharge. As a rule the doe is impregnated by the buck immediately after giving birth to young ; and at a period, estimated by different observers at from eight to twelve hours after impregnation, the ova are liberated from the ripe follicles.

At each period of ovulation, from three to nine ova are as a rule discharged from each ovary ; the several ova being set free, not absolutely at the same moment, but within a very short time of one another.

Although ovulation, or the discharge of ova from the ovaries, usually occurs a few hours after impregnation, and is probably stimulated by this, it should be regarded as an essentially independent act, a point of view that will be more fully considered in the next chapter.

5. Fertilisation

Fertilisation appears to occur in the rabbit, as a rule, from eight to twelve hours after copulation ; the interval being due, not to the time taken by the spermatozoa to travel up the uterus and oviduct, for this is effected, according to Hensen, in from a quarter of an hour to two hours ; but to the fact that the discharge of ova from the ovary does not take place until eight to twelve hours after copulation.

The act of fertilisation is effected, as a rule, directly after the eggs enter the oviduct : and, in eggs taken from the upper part of the oviduct, spermatozoa may be seen in considerable numbers imbedded in the zona radiata, or lying in the space between the vitelline membrane and the egg, formed by the shrinking of the latter.

The details of the process of fertilisation have not been accurately determined in the rabbit. Fusion of a spermatozoon with the female pronucleus has been seen by Van Beneden ; and there is no reason for supposing the process to differ from what is known to occur in other animals.


The Early Stages of Development

It will be convenient to deal, in the present section, with the changes undergone by the egg up to the end of the seventh day. During the first three days the egg is travelling down the oviduct, and passing through the stages of segmentation ; at the end of the third day it passes into the uterus, and undergoes further changes, consisting chiefly in the establishment of the germinal layers, and in preparations for the attachment of the ovum to the uterus. Up to the end of the seventh day the ovum lies freely in the uterus, and there is no trace of the embryo, which does not commence to form until the early part of the eighth day.

In estimating the age of rabbit ova, or embryos, it is customary to date from the time of copulation, which can always be determined with precision ; and this method of computation will be adopted here. As the eggs are not discharged from the ovary, or fertilised, until from eight to twelve hours after this event, the actual time during which developmental changes have been proceeding will be less than the stated periods by this amount.

1. Segmentation of the Egg

Segmentation is effected while the egg is travelling down the oviduct towards the uterus. During its passage it becomes surrounded by a thick layer of albumen, formed of concentric layers secreted by the walls of the oviduct. The egg itself, on entering the uterus at the close of segmentation, is practically the same size as the unfertilised egg, in reality slightly smaller than this ; but owing to the layer of albumen, which may be thicker than the diameter of the egg itself, it appears on a superficial examination to have increased considerably in size.

Segmentation commences, according to Van Beneden, some ten or twelve hours after fertilisation is effected, i.e. from eighteen to twenty-four hours after copulation, and is continued during the next two days. About the seventieth hour, or the end of the third day from the time of copiilation, segmentation is completed, and the ovum enters the uterus.

In segmentation, the first cleft (Fig. 136) divides the egg into two ovoid cells, which are nearly, but according to Van Beneden not absolutely, equal in size.

After a pause of about four hours, each of these cells again divides into two, giving in all four cells, which from the first are approximately spherical in shape. Each of these four then divides, giving eight in all, of which the four derived from the smaller of the first two cells are slightly smaller than the other four.


The larger cells now become grouped together in the centre, while the smaller cells form a cap lying on these, and partially inclosing them. In the later stages, the smaller outer cells divide rather more rapidly than the larger cells, and inclose these more completely ; and at the close of segmentation, about the seventieth hour, when the ovum passes from the oviduct into the uterus, it consists of a central solid mass of rather larger and more granular cells (Fig. 138, CD), almost completely surrounded by a layer of rather smaller and more transparent cells, slightly flattened at their outer ends (Fig. 138, cc) ; the larger cells being visible on the surface at one spot only.



FIG. 136. A Rabbit's Ovum from the middle of the length of the oviduct, about twenty-two hours after copulation, showing division of the ovum into two cells. (After Bischoff.) x 200.

CB, blastomere or segmentation cell. MO, spermatozoon imbedded in the zona radiata. N, nucleus. Z, zoua racliata.

FIG. 137. A Eabbit's Ovum from the lower end of the oviduct, about the middle of the third day ; showing the morula stage, shortly before the completion of segmentation. (After Bischoff.) x 200.


In the size of the eggs there is a close agreement between the rabbit and Amphioxus ; the rabbit's ovum measuring on an average 0' 1 1 6 mm. in diameter, and that of Amphioxus measuring 0-104 mm. The two eggs agree also in undergoing complete or holoblastic segmentation, and in the blastomeres, or cells formed by segmentation, differing very little from one another in size.

The comparison, however, must not be pushed too far. The actual arrangement of the cells is entirely different in the two cases : the rabbit's ovum does not pass through a gastrula stage (cf. Figs. 15 and 16) ; and there is no stage in the development of Amphioxus similar to that represented for the rabbit in Fig. 138.


In the spreading of the smaller cells over the larger ones, the rabbit and the frog appear to agree ; but the details of the process have not been accurately determined in the rabbit's ovum, and it is doubtful how far the correspondence is a real one.



FIG. 138. A Rabbit's Ovum seventy hours after copulation, taken from the lower end of the oviduct just before entering the uterus, and showing the condition at the close of segmentation. (After Van Beneden.) x 200.

FIG. 139. A Rabbit's Ovum seventy-five hours after copulation, taken from the uterus, and showing the first stage in the formation of the blastodermic vesicle. (After Van Beneden.) x 200.

CC. outer layer of cells. CD, inner mass of cells. CV, cavity of blastodermic vesicle.


2. The Blastodermic Vesicle

On entering the uterus, at the end of the third day, the ovum has the structure shown in Fig. 138 and described above. Itisspherical in shape, with a diameter averaging O09 mm., i.e. is slightly smaller than the unfertilised egg. It is surrounded by the vitelline membrane and zona radiata as before ; and outside the latter are the concentric layers of albumen, which are deposited round the egg during its passage along the oviduct, and which have a total thickness of about O'l mm.

From three to nine ova are usually discharged from the ovary at each period of ovulation. These enter the uterus almost simultaneously, and at first lie close together at its proximal end. As' development proceeds the} T gradually become spread out along the uterus, at approximately equal intervals ; each ovum lying in a special dilatation of the uterus, to the wall of which it becomes attached during the eighth day.

Very shortly after the egg enters the uterus, and in some cases before it leaves the oviduct, the smaller outer cells grow completely round the larger inner cells, which from this time they surround on all sides.

The outer layer of cells now begins to grow rapidly ; the central or inner cells remaining attached to the outer layer at one spot, but becoming separated from it at all other parts. By about the seventy-fifth hour, i.e. four or five hours after entering the uterus, the ovum has acquired the structure shown in Fig. 139 : the outer layer of cells, CC, forms a hollow ball, about 0'12 mm. in diameter, to the inner surface of which the mass of inner cells.



FIG. 140. Section of the blastodermic vessel of a Rabbit at the end of the fourth day. (After Van Beneden.) x 250.

CC, outer layer of cells. CD, inner lenticular mass of cells. CV, cavity of the blastodermic vesicle.

CD, is attached at one spot, the rest of the cavity of the ball, cv, between the outer and inner cells, being filled with fluid.

The growth of the ball, or blastodermic vesicle, as it is now termed, proceeds rapidly ; and by the end of the fourth day, i.e. about twenty-four hours after entering the uterus, the structure and proportions are as represented in Fig. 140. The vesicle is still spherical, measuring on an average about 0'28 mm. in diameter. It consists of an outer wall of flattened polygonal cells, CC, formed from the smaller, outer cells of the previous stages, to the inner surface of which is attached at one pole the mass of inner cells, CD. This mass of inner cells is now flattened out into a lenticular shape ; thicker and more compact in the middle, where the cells are two or thi'ee deep, and polygonal from mutual pressure ; and thinning towards its margins, where the cells are in a single layer, less closely opposed to one another, and irregular or even amosboid in form. The vitelline membrane is no longer recognisable : the zona radiata is still present, but, like the outer albuminous investment, is greatly reduced in thickness.

During the fifth and sixth days, the blastoderm ic vesicle remains spherical or nearly so in shape, and continues to increase rapidly in size. By the end of the fifth day it measures about 1-5 mm. in diameter; and by the end of the sixth day, 3 to 3*5 mm.

On the seventh day it becomes ellipsoidal in shape, and by the end of this day (Fig. 143) it measures from 4'5 to 5 mm. in length by 3'5 to 4 mm. in width. Up to the end of the seventh day the several blastodermic vesicles lie quite freely within the uterus, but become gradually spaced out along this, and take up the positions they will retain during the remainder of their development.

The measurements given above must be regarded as appi-oximate only ; the several blastodermic vesicles in the same uterus vary within certain limits, those lowest down being the largest and most advanced in development ; and one or two at the proximal end of the uterus, nearest to the oviduct, being almost invariably smaller and less developed than the others.

3. The Germinal Layers

During the fifth, sixth, and seventh days, important changes occur in the structure of the wall of the blastodermic vesicle, leading to the establishment of the three germinal layers, epiblast, hypoblast, and mesoblast, from which the several parts of the embryo are formed.

These changes more especially concern the part of the wall of the vesicle to which the lenticular mass of inner cells (Fig. 140, CD) is attached ; and to this part, which at the end of the fourth day is the only portion in which the wall of the vesicle is more than one cell thick, the name embryonal area may be given, as it is from the central portion of this that the embryo is developed.

The mode of formation of the germinal layers in the rabbit has been very differently described by different observers, and there are several points, even of primary importance, that are as yet imperfectly understood. The following description is based on the independent observations of Rauber and of Kolliker, which appear to be the most exact ; but the account, though consistent in itself, makes it very difficult to establish any comparison between the mode of formation of the germinal layers in the rabbit and that occurring in other Vertebrates, or even in other Mammals ; and it seems not at all improbable that further investigation may necessitate considerable modification in the interpretation to be put upon the appearances described.

The great length of time that is occupied in the process, as compared with the chick or frog, for example, is remarkable, and may perhaps be taken as an indication that the actual mode of development is a much modified one.

The fourth day. At the end of the fourth day, as already described, the wall of the blastodermic vesicle is one cell thick, except in the embryonal area, where cells of two kinds are present (Fig. 140).

The fifth day. During the fifth day, the cells of the outer layer become thinner and larger ; they also increase in number, by division, as the blastodermic vesicle grows larger. In the embryonal area the cells of the outer layer have the same characters as in other parts of the vesicle.

The granular cells forming the inner layer of the embryonal area, on the other hand, undergo important changes. They increase in number by repeated division ; they become smaller in size ; and they extend further round the interior of the vesicle. But the most important change is that they become arranged in two layers : (i) an upper layer of cells with large nuclei, rather wider than they are long, and closely fitted together at their edges so that the outlines of the cells are difficult to determine ; (ii) a lower layer of very thin flat pavement cells, similar to those of the outer laver of the vesicle, but slightly smaller ; this lower layer extends at its margin some distance beyond the edge of the upper or thicker layer.

Three regions may, therefore, be distinguished in the wall of the blastodermic vesicle of the rabbit on the fifth day.

(i) The embryonal area is a circular patch about 0-48 mm. in diameter, in which three lay era of cells are present (Fig. 141) ; an upper layer, CC, of thin pavement cells ; a middle layer. E, of much larger, almost cubical cells ; and a lower layer, H, of thin pavement cells, very similar to those of the upper layer. Each of these three layers is one cell thick ; and the threelayered condition is brought about by the splitting of the inner mass of cells of the fourth day (Fig. 140, CD) into two, which become respectively the middle and lower layers of the fifth clay.

(ii) Surrounding the embryonal area is a border, varying in width in different specimens, in which the wall of the vesicle consists of two layers, as seen at the margin of Fig. 141. These two layers correspond to the upper and lower layers of the three present in the embryonal area ; and the two-layered condition is brought about by the lower or innermost layer, H, extending beyond the margin of the embryonal area.

(iii) All the rest of the blastodermic vesicle, at this stage about four-fifths of the whole periphery, consists of a single layer of cells, the outermost layer, CC, of the embryonal area (cf. Fig. 140).

With regard to the ultimate fate of these layers, it may be mentioned at once that in the embryonal area, according to Rauber and Kolliker, the uppermost layer of cells, CC, often spoken of as Rauber's layer, disappears altogether ; the middle layer, E, becomes the epiblast ; and the lower layer, H, becomes the hypoblast ; so that, according to these observers, both epiblast and hypoblast are formed from the inner mass of cells of the fourth day.

This interpretation involves very considerable difficulties, and will not improbably require revision. The disappearance of Rauber's layer from the embryonal area, and its persistence as the outer wall of the vesicle in other parts, together with the derivation of both epiblast and hypoblast from the original inner layer of cells, are difficult to reconcile with the course of development in other Mammals; and further investigation is much needed on these points.


The sixth day. By the end of the sixth day, the blastodermic vesicle has a diameter of 3 to 3 - 5 mm., and the embryonal area, which is still approximately circular in outline, measures 0'75 mm. across.

In the embryonal area the upper layer of cells, or Rauber's layer, is thinner than before, and very difficult to recognise in sections. The middle layer of cells, or epiblast (cf. Fig. 141, E), is rather thicker than before, owing to a change in the shape of the individual cells, which are now columnar in place of being cubical. The lower layer, or hypoblast, consists, as before, of a single layer of ilat tenet! pavement cells, thickened in their centres by the nuclei, but very thin at their margins.

Beyond the embryonal area, the lower layer, or hypoblast, has extended further round the vesicle than before, so that it now lines about a third of the entire vesicle ; the wall of the remaining two-thirds still consists of a single layer of flattened cells. continuous with those forming Rauber's layer.

The seventh day. During the seventh day, and often before the close of the sixth, the blastodermic vesicle loses its spherical


FIG. 14:5. The blastodermic vesicle of a Rabbit at the end of the seventh day, seen from above. (Modified from Kolliker.) x 12.


the "


>. mi 1 uiasiouermic vesicie 01 a nauuu ai uie enu 01 TIIU s-e day, seen from above. (Modified from Kolliker.) x 12.

AD. embryonal ami. AGr, wall of blastodermic vesicle. "M", dotted line iivl lie boundary of the mrsoblast. PS, primitive streak.


FIG. 144. The embryonal area of a Rabbit at the middle of the eighth day. (Modified from Kolliker.) x 12.

NF. neural fold. NQ-, neural groove. PG, primitive groove. PS. primitive streak.

shape, and becomes ellipsoidal (Fig. 143). The average dimensions of the entire vesicle at the end of the seventh day are from 4'5 to 5 mm. in length, by 3*5 to 4 mm. in width; but individual specimens may considerably exceed these limits.

The embryonal area (Fig. 143, AD) is now distinctly pyriform in outline, measuring on an average 1*5 mm. in length, by 1 mm. in width. Its longer diameter corresponds to the axis of the blastodermic vesicle, and, as a rule, to that of the uterus as well. From their relations to the embryo at a later stage, the broader end of the embryonal area may be called the anterior end, and the narrower one the posterior end.

As regards the structure of the embryonal area, Rauber's layer has disappeared almost completely ; a few individual cells may still be recognised here and there, but there is no longer a continuous stratum of cells. In consequence of the disappearance of Rauber's layer (cf. Fig. 141), the embryonal area now consists of only two layers of cells : (i) the epiblast, or former middle layer, which now becomes the superficial layer, consists, as before, of a single layer of short columnar cells ; it thins towards the margin of the embryonal area, and at its margin is said to become continuous with the outer layer of cells, or epiblast cells of the rest of the blastodermic vesicle : (ii) the hypoblast, in the embryonal area, has the same characters as before ; beyond the embryonal area, it has now extended about half way round the inner surface of the blastodermic vesicle.

The blastodermic vesicle at the end of the seventh day is, therefore, an ellipsoidal sac filled with fluid. Its wall consists, in the upper half of the vesicle, of two layers of cells, epiblast and hypoblast ; in the lower half, of a single layer, the epiblast alone. In the middle of the upper half of the vesicle is the embryonal area, which is also two-layered, but in which the epiblast differs from that of the rest of the vesicle in consisting of columnar instead of pavement cells,

4. The Primitive Streak and the Mesoblast

Towards the close of the seventh day, the primitive streak appears. This structure, which in the mode of its formation, and in its relations to other parts, agrees closely with that of the chick, is at first an axial thickening of the epiblast at the posterior, or narrower, end of the embryonal area. It rapidly lengthens, and by the end of the seventh day (Fig. 143, PS) it extends, as a linear opacity, along about two-thirds of the length of the area, having a faint longitudinal groove, the primitive groove, along its dorsal surface.

Transverse sections at this stage (Fig. 142, rs) show that the primitive streak is formed by proliferation of cells from the under surface of the epiblast, in the median plane.

The mesoblast. The cells of the primitive streak spread out, beyond the margins of the thickened streak itself, as two thin lateral sheets of cells (Fig. 142. M), which lie between the epiblast and hypoblast, and which give rise to the middle germinal layer or mesoblast. In the primitive streak itself the cells are spherical and closely compacted ; but in the lateral mesoblast sheets the cells are more loosely arranged, and are stellate in shape.

The layer of mesoblast spreads rapidly, both laterally and posteriorly ; at the end of the seventh day, its limits are indicated by the shaded area bounded by the dotted line, M, in Fig. 143, a figure that may with advantage be compared with Fig. 107, which shows the corresponding stage in the development of the chick.

While it is certain that the mesoblast in the posterior part of the embryonal area of the rabbit, i.e. in the region of the primitive streak, arises in the manner just described, by proliferation of cells of epiblastic origin, it is by no means clear that the whole of the mesoblast is formed in this- way ; and, although further observations are wanted on the point, it seems probable that in front of the primitive streak, in the part of the embryonal area in which the embryo will appear, the mesoblast arises, as in the chick, by budding off of cells from the hypoblast.

General History of the Development of the Rabbit Embryo

In the preceding section the development of the rabbit's ovum has been followed up to the end of the seventh day, that is, up to a point corresponding to that reached by a hen's egg about the sixteenth hour of incubation. At this stage all three germinal layers, epiblast, mesoblast, and hypoblast, are established ; a primitive streak and primitive groove are present ; but there is as yet no trace of the embryo itself.

It will be convenient to give, in the present section, a brief summary of the mode of formation, and of the general course of development of the embryo, before considering in detail the history of the several systems and organs.

1. The Formation of the Embryo

The embryonal area of the blastodermic vesicle of the rabbit at the end of the seventh day (Fig. 143. AD) corresponds very closely, as just noticed, with the area pellucida of a hen's egg about the sixteenth hour of incubation.

The formation of the rabbit embryo is also effected in very similar fashion to the chick. The embryonal area increases in size, especially by growth at its anterior end. Immediately in front of the primitive streak a neural groove (Fig. 141, XG) is



FIG. 145. A Rabbit Embryo at the end of the ninth day. The entire blastodermic vesicle is represented, with the embryo in situ, as seen from the dorsal surface. (Cf. Fig. 146, which represents an embryo of the same age in sagittal section.) x 10.

AN', proamnion. BM, mid-brain. E', horse-shoe shaped patch of thickened epiblast, by which the blastodenuic vesicle is attached to the wall of the uterus (cf. Fig. 169). MS, mesoblustic somite or protovertebra. R, right half of heart. SI, sinus teriuiualis. TA, allantois.

formed, bordered by neural folds, XF, which speedily unite, converting the groove into a tube. This tube becomes the central nervous system, and in its anterior or cerebral part the several brain vesicles are early established (Fig. 145).

By means of head, tail, and side folds the embryo is constricted off from the rest of the blastodermic vesicle, in a manner practically identical with that in which the embryo chick is constricted off from the yolk-sac (cf. Figs. 145, 146, and 110, 112).

By the end of the ninth day the rabbit embryo (Figs. 145, 14G) has acquired shape, structure, and proportions agreeing very closely with those of a chick embryo of about the twenty-sixth hour, with which it also corresponds almost exactly in size.

Up to this stage the embryo has been practically straight



FIG. 146. A median longitudinal, or sagittal, section through a Rabbit Embryo and blastodermic vesicle at the end of the ninth day. {Cf. Fig. 145.) (In part after Van Beneden and Julin.) x 10.

AN, tail fold of amnion. AN', proamiiion. BM.niid-brain. C, extra-embryonic part of tbe eceloiu or body-cavity. CP. pericardia! cavity. E, epi blast. E', thickened epiblast by which the blastoderniic vesicle is attached to the uterus (cf. Fig. 169). EK, epiblastic villi. GF. 1'oiv-jrut. GH. liiiKl-irut. QT, mid-gut. H. hyiblast. M, mesoblast. SI, Mini* terminalis. TA. alhmt<>i>. YS, cavity of yolk-sac,' or blastodenuic vesicle.

(Fig. 146), lying with its dorsal surface upwards, towards the wall of the uterus, and its ventral surface downwards towards the yolk-sac. From this time, however, the dorsal surface of the embryo grows more rapidly than the ventral surface, and the whole embryo in consequence becomes strongly flexed. By the end of the tenth day (Fig. 147), while the middle portion of the body, to which the yolk-stalk is attached, remains in the same position as before, the head and neck, which have greatly increased in size, are bent downwards at right angle* to the trunk, and, pushing down the wall of the yolk-sac before them, appear to project into this latter : the head and neck are, however, really separated from the cavity of the yolk-sac, as shown in Fig. 147, by the wall of the sac itself. The hinder or tail end of the embryo, the basal part of which is alone shown in


FlG. 147. A Rabbit Embryo and blast odermic vesicle at the end of the tenth day. The embryo is represented in surface view from the right side, the course of the alimentary canal being indicated by the broad dotted line ; the blastodermic vesicle is shown in median longitudinal, or sagittal section. The greater part of the tail, which in the natural condition is twisted spirally, has been removed. (In part after Van Beneden and Julin.) x 10.

AN', proamnion. AX, amnionic cavity, between the inner or true amnion and the embryo. C, extra-embryonic part of the coalom or body-cavity. E, epiblast. HI', thickened



Fig. 147, has also grown considerably, and is wrapped spirally round the stalk of the allantois.

By the twelfth day the embryo has acquired the form shown


iu Fig. 148. The several divisions of the brain are clearly recognisable, as are also the nose, and the eyes and ears. On the



FIG. 148. A Rabbit Embryo and fcetal appendages at the end of the twelfth day. The embryo is represented in surface view from the right side ; the yolk-sac and foetal membranes are shown in median longitudinal, or sagittal section. The hind-limb and part of the tail have been removed to allow the yolk-stalk and allantoic stalk to be fully seen. In part after Van JJeneden and Julin. x 8.

AX, amnionic cavity, between the inner or true amnion and the embryo. C, CX, extra-embryonic part of the coeloni or body-cavity. E, epiblast. E', ectoplacenta, or thickened part of the epiblast, from which the placenta is formed. EK, epiblastio villi. H, hypoblast. M, mesoblast. SI, sinus terminalis. TA, cavity of allantois. Y"S, cuvity of yolk-sac or blastodermic vesicle.


sides of the head and neck the visceral arches and clefts are well seen ; and both fore and hind limbs have attained considerable size, and show indications of division into their several segments.

The twelfth-day rabbit embryo corresponds closely in form and in structure to a chick embryo of the middle of the sixth day, and is of very nearly the same actual size. The chief points of difference between the two are the much smaller size of the brain and of the sense organs, more especially the eye, in the rabbit.

The first trace of the neural groove appears in the chick embryo about the eighteenth hour of incubation, and in the rabbit embryo early on the eighth day. Starting from this stage, the rate of development is approximately the same in the two embryos ; the twelfth day rabbit embryo corresponding tot-he chick embryo about the middle of the sixth day.

By the twentieth day the rabbit embryo has attained the shape and size shown in Fig. 149 ; in grade of development, and also in actual dimensions, it corresponds very closely to a chick embryo of the twelfth day .

The young rabbit is born on the thirtieth day, i.e. about twenty-two days from the time of first appearance of the neural groove, the earliest formed organ in the body. The chick is hatched on the twenty-first day of incubation, or rather more than twenty days from the same starting-point. The young rabbit at birth is of considerably greater bulk than the chick on hatching, but is in a far more helpless condition ; the eyelids are still united together, and the young animal is quite incapable of looking after itself, and would perish but for the supply of milk afforded it by the mother.

2. The Yolk-sac

The yolk-sac is the extra-embryonic portion of the blastodermic vesicle ; i.e. the part which is left after the embryo is constricted off by the head, tail, and side folds.

The yolk-sac (Figs. 146, 147, 148, YS), though corresponding in its mode of formation, and in its relations to the embryo, with the yolk-sac of the chick embryo (cf. Fig. 100), differs from this latter in one very important respect. The yolk-sac of the bird is filled with food matter for the nutrition of the embryo, and affords the supply of nourishment at the expense of which the


FIG. 149. A Rabbit Embryo of the twentieth day, seen from the right side. The rows of spots round the nose and above the eye, and the single large spot below the eye, represent hair follicles, the last -mentioned one being of especial size, x 1.


whole development is effected. The yolk-sac of the Mammal, 011 the other hand, is a thin-walled vesicle, containing fluid, but 110 food matter.

Hence the causes that led to the formation of a yolk-sac in the bird, i.e. the necessity of constricting off the active from the inactive part of the egg in order to avoid undue distortion of the embryo, will not come into play in the case of the Mammal ; and the formation of a yolk-sac by the rabbit embryo must be explained as due to an inherited tendency, and compels us to infer that Mammals are descended from ancestors which produced large eggs, provided with much foodyolk. Further evidence in support of this view has already been given in the earlier portions of this chapter.

With regard to the structure of the yolk-sac of the rabbit embryo, it will be seen in Fig. 140 that the wall of the upper portion, rather less than half the entire surface, consists of all three embryonic layers epiblast, mesoblast, and hypoblast excepting only a small patch (Figs. 145, 140, AN'), immediately in front of the head of the embryo, which will be referred to shortly. The wall of the lower half of the yolk-sac contains no mesoblast, but is formed of epiblast and hypoblast alone.

In the mesoblast of the upper half of the yolk-sac, bloodvessels are present, forming the vitelline circulation, or circulation of the vascular area (Fig. 145). The margin of this vascular area, or, what is the same thing, the margin of the mesoblast, is indicated by a circular vessel, the sinus terminalis (Figs. 145, 140, 147, 148, si), into which the vitelline artery opens, and from which the blood is distributed over the vascular area before it is returned to the heart by the vitelline veins.

By the downward projection of the head of the embryo on the tenth day (Fig. 147), the upper wall of the yolk-sac becomes driven ventralwards, and during the succeeding days, as the embryo gets bigger (Fig. 148), this doubling up of the yolk-sac becomes more and more marked. By the thirteenth day the two layers, vascular and non-vascular, are almost in contact with each other, and the cavity of the yolk-sac is practically obliterated.

The outer or non-vascular wall, which is in contact with the wall of the uterus (cf. Fig. 170, YL), now breaks down and becomes absorbed. Portions of it persist for a time ; but by about the sixteenth day it has practically disappeared, and the vascular, or original upper wall of the yolk-sac, comes into contact with the wall of the uterus, the hypoblast of the yolk-sac lying in contact with the uterine epithelium.

About the eighth day, irregular epiblastic buds (Figs. 146, 117, KK) nrir-fe from the surface of the lower, or non-vascular, half of the yolk-sac. These acquire close attachment to the mucous membrane of the uterus, and aid in fixing the blastodermic vesicle in position, while it is possible that they have also some nutritive function. They begin to degenerate about the ninth day, and by the fourteenth or fifteenth day have disappeared.

3. The Amnion

The amnion of the rabbit, while agreeing in most respects with that of the chick, differs from this in the prominent share taken by the tail-fold, which, as was first pointed out by Van Beneden and Julin, practically forms the whole amnionic covering of the embryo.

On the ninth day, as already mentioned, there is, immediately in front of the head of the embryo, a patch of the blastoderm, roughly circular in outline (Figs. 145, 146, AX'), into which the rnesoblast does not yet extend, and which therefore consists of epiblast and hypoblast alone. This patch is termed the proamnion, and corresponds to the similarly named structure in the chick.

The rapid growth of the head of the embryo forwards, and then downwards, depresses the pro-amnion so as to form a deep pocket, projecting into the yolk-sac. This is a well-marked feature on the tenth and eleventh days (Fig. 147, AN'), but from the twelfth day onwards it becomes less obvious (Fig. 148), owing to the general depression of the upper wall of the yolksac which is then occurring.

The pro-amnion, as a special part of the wall of the yolksac, has only a temporary existence. The mesoblast gradually invades it from the sides, spreading inwards between the epiblast and hypoblast, and, on the three-layered condition being definitely attained, the pro-amnion as such ceases to exist.

The amnion itself is formed almost entirely by the tail-fold, aided to a slight extent by the side-folds. The tail-fold of the amnion (Fig. 146, AN) is formed immediately behind the tail end of the embryo, partly by depression of the embryo into the yolk-sac, and partly by the actual uprising of a fold of the souiatopleure, or body wall.

After it is once started, the amnion grows rapidly, and by the end of the tenth day has spread forwards so as to roof over the whole body of the embryo. In front of the embryo it meets and fuses with the somatopleure, at the anterior border of the pro-amnionic pit (Fig. 147).

Apart from the prominent share taken by the tail-fold, the formation and relations of the arnnion are practically the same in the rabbit as in the chick. As the amnion is a fold of somatopleure (Figs. 146, 147), the space between its inner and outer layers is necessarily continuous, as in the chick, with the coelom or body cavity of the embryo.

4. The Allantois

The , allantois arises, on the ninth day (Fig. 146, TA), as a hollow diverticulum from the ventral surface of the hinder end of the alimentary canal, appearing almost like a posterior prolongation of the embryo itself. It consists, at first, of a thick wall of mesoblast, in which the allantoic vessels develop very early, and a lining of hypoblastic epithelium ; and from its first appearance it is in very close relation with the amnion. or actually continuous with this (Fig. 146).

As the amnion extends forwards, the allantois grows with it, spreading rapidly between its two layers, and over the back of the embryo (Fig. 147, 148, TA). Owing to its early fusion with the outer layer of the amnion, the upper surface of the allantois lies practically in contact with the wall of the uterus.

The cavity of the allantois is at first small, but from the tenth to the twelfth days it enlarges very greatly (Figs. 147, 148, TA).

5. The Placenta

The placenta, is the organ through which the embryo receives, from the blood of the mother, the nutriment by which it is enabled to develop. It is a structure of great importance and great complexity ; the mode of its formation will be dealt with fully at the end of this chapter, but a brief outline may be given here, in order to render its relations to the blood-vessels and other organs of the embryo more intelligible.

Up to the seventh day the blastodermic vesicle lies quite freely in the uterus (Fig. 108), but towards the end of the seventh day it begins to acquire adhesions to the uterine wall. These are effected partly by the small epiblastic villi of the lower pole of the vesicle (Fig. 146, EK), but principally by the epiblast cells of the vascular area : these latter proliferating freely over a horse-shoe-shaped patch (Fig. 145, E'), which surrounds the sides and hinder end of the embryonic region ; and growing out into irregular tags and processes, which adhere firmly to the wall of the uterus. By the ninth day (Figs. 145, 146, and 169), this adhesion has become so firm, that, if the blastodermic vesicle is pulled away from the uterus, the thickened epithelium over this horse-shoe area is torn from the vesicle and remains attached to the uterine wall.

By the tenth day (Fig. 147), the allantois has come into extensive contact with the wall of the blastodermic vesicle beneath this area of attachment ; and the blood-vessels of the allantois are thus brought very close to the uterine vessels of the mother. By a further series of changes, which will be fully described later on in this chapter, the surface of contact between the maternal and foetal blood-vessels is greatly increased, and the highly complicated structure of the placenta is gradually elaborated (cf. Fig. 170).

Development of the Nervous System

1. General Account

In the rabbit, as in the chick and other Vertebrates, the nervous system is established very early. The neural groove (Fig. 144, NG) appears, about half way through the eighth day, as a shallow longitudinal depression, in front of the primitive streak, and bordered laterally by the neural folds.

The neural groove rapidly increases, both in length and in depth. By the end of the ninth day (Fig. 145) the lips of the groove have met and fused along the greater part of their length, though still remaining separate at both the anterior and posterior ends. The distinction between the wider anterior part, or brain, and the narrower posterior portion, or spinal cord, is very evident ; and the vesicles of the fore-brain, mid-brain, BM, and hind-brain are already well established.

The general history of the development of the nervous system, both central and peripheral, of the rabbit is closely similar to that of the chick, and it will be only necessary to describe in the present section the points of more special interest, and in particular those characteristic of Mammals as contrasted with Birds.

2. The Brain

Cranial flexure commences towards the end of the ninth day (Fig. 146), before closure of the neural canal is completed ; and proceeds rapidly. By the tenth day (Fig. 117) the brain and spinal cord are closed along their whole length; cranial flexure is strongly pronounced ; and the head of the embryo, mainly owing to the rapid growth of the brain, has acquired a shape, and proportions, similar to those of a chick embryo towards the close of the fourth day of incubation.

By the twelfth day (Fig. 161) the head has increased considerably in size, and, when the embryo is viewed from the side, appears to be bent twice at right angles ; the first bend being near the junction of the brain and spinal cord, opposite the reference line H Y in Fig. 161 ; and the second bend being marked by the mid-brain, BM, which forms the most prominent part of the brain at this stage.

Sagittal sections of twelve-day embryos (Fig. 150) show that flexure has really taken place to a far greater extent than is apparent from the surface. Following the floor of the brain from behind forwards, there is first, at the junction of spinal cord and mid-brain, between the reference lines TH and CH in Fig. 150, a rather sharp bend, ventralwards, of nearly 90 ; this is corrected a little further forwards by a second and more gradual bend dorsalwards, at the level of the reference line PT. At the base of the mid-brain, BM, there is a very sharp and sudden bend of about 180, by which the infundibulum, IN, and the floor of the hind-brain are brought almost into contact with each other. In front of the infundibulum the floor of the brain again bends dorsalwards, and nearly at right angles.

These flexures are even more strongly marked in the later stages of development, the angles formed by them becoming sharper and more pronounced. This is well shown in Fig. 151, which represents the condition of the brain on the eighteenth day, as seen in sagittal section. The extreme sharpness of the bend at the junction of the spinal cord and brain, between the reference lines RP and 01 in Fig. 151, is very characteristic of mammalian embryos at this stage ; while the sharp bend at the base of the mid-brain is quite as conspicuous as in the earlier stage.



FIG. 150. A median longitudinal, or sagittal section through a Babbit Embryo at the end of the twelfth day. The section is a strictly median one except in two respects : the cerebral hemisphere of the left side has been introduced in order to render the figure more complete; and the Wolffian body and ureter of the right side. The terminal portion of the tail has been removed. (Compare Fig. 161 for a surface view of an embryo of the same age.) x 14.

BF, cavity of fore-brain or thalamcncephalon. BH, cavity of hind-brain, or fourth ventricle. BL, cerebellum. BM, cavity of mid-brain. BS, cavity of cerebral hemisphere, or lateral ventricle. CH, uotochord. Q-P, post-anal fjut. IN, finger-like process of infundibuluni. KG, Wolffian duct. KI), ureter. KM, Wolffiaii body. LE, epiglottis. LG, lung. LR, trachea. PN, pineal body. PT, pituitary body. B,S, sinus venosus. RT, trillions arteriosus. B,V, ventricle of heart. T, glottis. TA, stalk of allantois, cut short. TO. cloaca. TH, thyroid body. TO, oesophagus. TP, pharynx. "W, liver. WD, bile duct, YK, yolk-stalk, cut short.


The general relations of the brain to the head are much the same in the rabbit embryo as in the chick. In the early stages (Figs. 147, 148, and 150) the brain forms practically the whole of the head, and determines its shape almost exclusively ; but in the later stages (Figs. 149, 151), as the parts of the face assume definite shape, and grow forwards to form the snout, the brain becomes thrown more and more on to the dorsal surface, and ultimately to the posterior part of the head, and takes a much less prominent share in determining the general contour.

In dealing with the several parts of the brain it will be convenient to commence with the thalamencephalon. and the structures developed from, or in connection with it.

The thalamencephalon (Fig. 150, UF) is the anterior cerebral vesicle, or fore-brain, of the early stages (cf. Figs. 145, 1 16). From it the optic vesicles arise as lateral outgrowths ; these appear very early, and attain some size before the roof of the fore-brain is closed (Fig. 1 15) ; their further development, and their conversion into the essential parts of the eyes, will be described in the next section of this chapter, p. 387.

The side walls of the thalamencephalon thicken very quickly, to form the optic thalami (Fig. 155, BU) ; and, owing to this thickening of its sides, the central cavity, or third ventricle, becomes reduced to a vertical cleft, very narrow from side to side. The anterior wall of the thalamencephalon remains thin, as the lamina terminalis (Fig. 151, BT), lying between the roots of the two cerebral hemispheres.

The roof of the thalamencephalon remains thin, consisting in the greater part of its extent of a single layer of epithelial cells, devoid of nervous elements of any kind. From this roof, rather behind the middle of its length, the pineal body arises about the twelfth day, as a hollow median papilla (Fig. 150, PN). This rapidly lengthens, forming a tubular and backwardly directed diverticulum of the brain. Its distal end dilates (Fig. 151, PX), to form a slightly expanded vesicle, from the sides of which irregular hollow outgrowths arise : at a later stage these outgrowths become solid, and separate completely from the stalk. In front of the pineal body the roof of the third ventricle,


FlG. 151. A median longitudinal, or sagittal section through the head of a Rabbit Embryo of the eighteenth day. (Compare Fig. 149 for a surface view of an embryo at a slightly later stage.) x 10.

BF, cavity of tbalamencephalon, or third ventricle. BH, cavity of medulla i)l>l(ingatii.or fourth ventricle 1 . BL, cerebellum. BM, cavity of mid-brain. BS, cavity of cerebral hemisphere, or lateral ventricle. BT, lamina tenuinalis. BY, cavity of olfactory lobe. CT, thyroid cartilage. ET, mesethmoid cartilage. F.I, first cervical or atlas vertebra. F.2. second cervical or axis vertebra. IN, infundibulum. LR,, trachea. LT. glottis. MC, Meckel's cartilage. M"S, central canal of spinal cord. OB. Imccal cavity. QI, odontoid process of axis vertebra. OX, supraoccipital cartilage. PF, jmsterior narial chaml)er. PL, palate. PN", pineal body. PT, pituitary body. RP. basilar plate. TN, tongue. TO, oeso])hagus. TP, ptiarynx. XA. choroid plexus of third ventricle. XB, ehoroid plexus of fourth ventricle.

which is here excessively thin, becomes thrown into folds, which hang down into the cavity of the ventricle (Fig. 151, XA). Between these folds blood-vessels pass in, from the vascular mesoblast outside the brain, and give rise to the choroid plexus of the third ventricle.

The floor of the thalamencephalon also remains thin, though not so thin as the roof. The anterior part of the floor is crossed by a shallow transverse groove, which is prolonged outwards into the optic stalks (Figs. 150, 151, and 155). The posterior part of the floor gives rise to the infundibulum. This is a median, thin-walled depression, from the hinder end of which a hollow finger-like diverticulum arises on the tenth day (cf. Fig. 150, IN); this diverticulum lies, from the first, in very close relation with the anterior end of the notochord, and with the pocket-like outgrowth from the stomatodasum (Fig. 150, PT), which gives rise to the pituitary body. This anterior end of the notochord is ultimately absorbed and obliterated ; but the infundibular diverticulum and the pituitary body remain in intimate relation throughout life ; the diverticulum forming what is spoken of, in the adult rabbit, as the posterior lobe of the pituitary body.

The further development of the pituitary body itself, whichmay conveniently be dealt with here, is as follows. The stomatoda\il diverticulum (Fig. 1 50, PT) dilates at its blind end, and gives off from this terminal dilatation hollow outgrowths ; these branch freely (Fig. 151, PT), but in the later stages of development become solid. The central dilated cavity of the pituitary body persists ; it retains its communication with the buccal cavity, through the tubular stalk, for some time. The formation of the palate (Fig. 151, PL) leaves the pituitary stalk in communication with the narial passage, but cuts it off from direct communication with the buccal cavity. In the later stages, the pituitary stalk loses its connection with the narial passage, and becomes obliterated.

The cerebral hemispheres arise, as in the chick, in the first instance as a median anterior prolongation of the thalamencephalon, which may be termed the vesicle of the hemispheres. This soon becomes divided by an inwardly projecting fold of its anterior wall into right and left lobes, which by further growth become the cerebral hemispheres ; the median anterior wall of the vesicle, between the bases of the hemispheres, persisting as the lamina terminalis.

From their mode of formation the hemispheres are necessarily hollow ; and their cavities, the lateral ventricles, retain throughout life their communications with the third ventricle through the foramina of Monro, a pair of apertures which are at first wide, but which gradually become reduced, by thickening of their lips, to narrow slits.

The cerebral hemispheres first become prominent about the twelfth day (Fig. 150, BS) ; from this date they grow actively,


-The brain dissected from above. Enlarged. (From Marshall and Hurst.)

C, lateral lobe of cerebellum. CA, pillars of cerebellum. CB, cut edge of velum mednllse posterius. CC, corpus callosum : the right half is removed.' CD, cut edge of corpus callosuni. CF, floccular lobe of cerebellum. CS, corpus striatum. F, anterior limit of body of foriiix. H, bippocampus major, M, medulla oblonpata. O, olfactory lobe. OP, anterior optic lobe. P, pineal body. V, fourth ventricle.

extending forwards, and still more rapidly backwards, so as to overlie and cover the roof of the thalamencephalon. and at a later stage the mid-brain as well (cf. Figs. 151 and 152).

The wall of each hemisphere is at first thin on all sides, and the cavity, or lateral ventricle, is consequently large (Fig. 151). The inner wall remains thin, but the outer wall (Fig. 152) thickens considerably in the later stages of development ; while the hinder ends of the hemispheres thicken still more, to form the corpora striata (Fig. 155, BI), a pair of prominent swellings, lying in front and to the outer sides of the optic thalami, BU, and separated from these by well-marked grooves.

The hippocampus major (Fig. 152,n) is a prominent curved ridge, projecting into the lateral ventricle, and extending round into its descending cornu ; it is really an inwardly projecting



FIG. 153. A longitudinal and vertical section of the brain of an adult Rabbit, taken jn the median plane. (From Marshall and Hurst.)

A, pituitary Ixuly. AC. anterior commissure. AF, anterior pillar of the fornix. in in the wall of the third ventricle. C, cerebellum. CA, corpus albicans. CC


!, optic chiiistna. ON, left optic nerve. P, pineal body. PC, posterior commissure. v ", JHIIIS Varolii. T. (posterior lobe of corpora quadrifreinina, or ' tcstis.' VA, velum ieilu]lw anteriiis, or valve of Vieusseiis. ~VP, velum meilullae postering. III. third ventricle. IV. fourth ventricle. V, fifth ventricle.


fold of the wall of the hemisphere, formed by a deep groove on the surface of its inner wall.

The choroid plexus of the lateral ventricle (Fig. 155, x) is a somewhat similar, but much thinner fold of the inner wall of each hemisphere, between the two layers of which blood-vessels, XD, pass in freely. It lies immediately below the hippocampal fold.

The commissural bands between the two hemispheres are very characteristic structures in Mammals, in which they attain a much higher development than in other Vertebrates. The most important of these are the corpus callosum, the fornix, and the anterior, middle, and posterior commissures of the third ventricle. Their development is complicated, and difficult to follow.

In front of the lamina terminalis, the two hemispheres extend forwards side by side, very close to each other (Fig. 152), but separated by a median cleft in which lies the connective tissue lamina from which the falx cerebri is formed. At the hinder end of this cleft, just in front of the lamina terminalis, the walls of the two hemispheres come in contact and fuse ; and from this fused patch, which is somewhat triangular in shape as seen in sagittal section, the commissural bands are formed. The corpus callosum (Fig. 153, cc), the most important of them, is formed from the dorsal part of the fused patch ; it develops from before backwards, the anterior end being formed first. The fornix, in which the fibres are mainly longitudinal in direction, is formed from the ventral part of the patch ; and the anterior commissure from its hinder end, just in front of the lamina terminalis. It is not quite clear whether the fifth ventricle (Fig. 153, v) is formed by the breaking down of the central part of the fused patch, or is merely a persistent part of the original cleft between the two hemispheres.

The surfaces of the hemispheres are at first smooth, and even in the adult rabbit are only slightly convoluted. The convolutions arise as foldings or grooves of the surface, extending to a greater or less depth, and are classed as primary or secondary according to whether they are folds involving the whole thickness of the wall of the hemisphere, or mere grooves in its substance.

The olfactory lobes appear, about the fourteenth day, as a pair of hollow outgrowths from the ventral surface of the anterior ends of the cerebral hemispheres ; by the eighteenth day (Fig. 151, BY) they have become prominent structures.

The mid-brain. In. the early stages, up to about the twelfth day (Fig. 150), the mid-brain is very imperfectly marked oft from the fore-brain ; later on (Fig. 151), the boundary between the two divisions becomes well defined.

As compared with the chick, the mid-brain of the rabbit is of rather smaller size, and less prominent : it is further distinguished by its tendency to grow backwards over the hindbrain, a tendency already present on the twelfth day (Fig. 150), but much more pronounced in the later stages, the posterior lobes of the mid-brain on the eighteenth day (Fig. 151) completely overlapping the cerebellum, BL.

The roof of the mid-brain gives rise to the corpora quadrigemina. A transverse furrow first appears, dividing it into a larger anterior, and a smaller posterior portion ; the anterior portion soon becomes divided, by a median longitudinal groove, into the anterior lobes of the corpora quadrigemina, or nates ; the posterior portion, overhanging the cerebellum, is not divided until a much later stage.

The floor of the mid-brain forms the very sharp bend at the base of the brain which has already been noticed (Figs. 150 and 151) ; as in the chick, it becomes greatly thickened on the formation of the longitudinal pillars of nerve fibres known as the crura cerebri (Fig. 154, cc), which connect the optic thalami and corpora striata with the hind brain.

The cerebellum is developed from the roof of the anterior part of the hind-brain, in much the same way as in the chick. On the tenth day (Fig. 147) a slight thickening is formed across the roof of the anterior end of the hind-brain ; by the twelfth day this has become more conspicuous (Fig. 150, BL), but is still only a slightly thickened transverse band. By the eighteenth day (Fig. 151, BL) it has increased considerably in thickness ; and, shortly after this stage, it becomes folded transversely on itself, as in the chick (cf. Fig. 116, BL). Secondary foldings appear on its surface, and the complicated structure of the adult cerebellum is gradually acquired.

Of the several parts of the adult cerebellum (cf. Fig. 152), the median lobe, or vermis, is the first to be formed ; the lateral lobes and floccular lobes appearing at a much later date.

Immediately in front of the cerebellum, between it and the mid-brain, the roof of the brain becomes extremely thin, forming the velum medulla anterius (Fig. 153, VA), which is ultimately reduced to a single layer of epithelial cells devoid of nervous elements.

The medulla oblongata is formed from the floor of the hind-brain, and from the part posterior to the cerebellum. The floor of the medulla oblongata remains thin in the actual midventral plane (Fig. 158) ; the lateral parts of the floor, and the sides as well, thicken very considerably. The roof of the fourth ventricle, as in the chick, widens out considerably (Fig. 158), and at an early stage becomes exceedingly thin. Immediately behind the cerebellum, the roof of the medulla remains comparatively smooth, as the velum medullas posterius (Fig. 153, VP) ; but a short way further back it becomes thrown into a complicated series of folds (Fig. 151, XB), which hang down into the fourth ventricle, and between the layers of which the bloodvessels penetrate in. lai'ge numbers to form the choroid plexus of the ventricle.

The walls of the medulla oblongata consist mainly of longitudinal fibres. The pons Varolii (Fig. 153 and 154, PV), the great transverse band of nerve fibres which connects the two halves of the cerebellum together, develops very late ; its position is indicated, about the eighteenth day, by the sharp rectangular bend in the floor of the medulla, opposite the cerebellum (Fig. 151).

Before leaving the brain, it should be noted that, in spite of the complicated foldings which various parts of it undergo, and the extreme thinness to which its walls are reduced in places, notably in the roof of the third, and in that of the fourth ventricle, the cavity of the brain remains a closed one, and its walls are not actually perforated at any place.

The membranes of the brain, i.e. the pia mater and dura mater, are connective-tissue structures, of mesoblastic origin.

3. The Spinal Cord

The development of the spinal cord of the rabbit need not be described in detail, as in all essential respects it agrees with that of the chick.

4. The Histological Development of the Brain and the Spinal Cord

This will be more fully dealt with in the chapter on Human Embryology.

In the spinal cord, the changes undergone are essentially similar to those in the chick. The original walls of the neural canal give rise mainly to the grey nervous matter, the innermost layer of cells forming the epithelial lining of the central canal. The white matter develops later ; in the spinal cord it appears on the eleventh day, the ventral and lateral bands of white matter being formed practically simultaneously. The central canal of the spinal cord remains a narrow vertical cleft until about the sixteenth day, when its dorsal part becomes obliterated, as in the chick, preparatory to the formation of the dorsal fissure.

In the medulla oblongata, the arrangement of white and grey matter is essentially the same as in the spinal cord, the white matter forming, about the eleventh day, on the outer surface of the grey matter ; in the later stages the relations between white and grey matter become much more complicated.

In the fore-brain the conditions are somewhat different. The walls of the hemispheres, which at first are very thin, become early differentiated into an outer layer of rounded elements, which later on give rise to grey matter, and an inner epithelial layer, which becomes the epithelial lining of the ventricle. About the sixteenth or seventeenth day, bands of white fibres grow upwards from the crura cerebri, through the optic thalami and corpora striata, and make their way between the two layers of the wall of the hemisphere ; while a little later a very thin superficial layer of white matter forms on the surface of the brain, outside the grey matter. In this way the characteristic distribution of white and grey matter in the hemispheres of the adult is brought about.

5. The Peripheral Nervous System

The general history of the peripheral nervous system is the same in the rabbit as in the chick ; but the earliest stages of development have not yet been worked out in such detail. By the ninth day both spinal and cranial nerves are established, and by the eleventh day (Fig. 165) all the principal branches of distribution are present.

The Cranial Nerves.

I. The olfactory or first cranial nerve. The time of first appearance of the olfactory nerve in the rabbit has not been definitely determined. The nerve is, however, clearly recognisable, as a short stem, connecting the cerebral hemisphere with the olfactory pit, before the olfactory lobe is formed.


II. The optic or second cranial nerve will be considered in the section dealing with the development of the eye, p. 387.


FIG. 154. The brain of an adult Rabbit from the ventral surface. The greater part of the left temporal lobe has been sliced off' horizontally. The planes of the three semicircular canals of the left side are indicated by the thick lines surrounding the floccular lobe of the cerebellum. (From Marshall and Hurst.) x 2.

CC, crus cerebri. CG, corpus genieulatum. D, descending coriui of left lateral ventricle. H, hippocampus major. LF, floccular lobe of cerebellum. LL, lateral lobe of cerebellum. OC, optic chiasina. OT, optic tract. P, pituitary body. PV, pons Varolii. SA. anterior vertical semicircular canal. STT. horizontal semicircular canal. SP, posterior vertical semicircular canal. T, temporal lobe of cerebral hemisphere.

I, olfactory lobe, with roots of olfactory nerves. II, optic nerve. Ill, third nerve or motor oculi. "IV, fourth nerve. V, trigeminal nerve. VI, sixtli nerve or abducens. VII. facial nerve. VIII, auditory nerve. IX, glosso-pharyngeal nerve. X, pnemnogastric nerve. XI, spinal accessory nerve. XII, hypoglossal nerve.

Ill, IV, and VI. The third, fourth, and sixth cranial nerves. There are no exact observations recorded 011 the development of these three nerves in the rabbit. From the time when they can be clearly recognised, about the eleventh day, their course and relations are the same as in the adult.

V. The trigeminal or fifth cranial nerve. This nerve can be recognised on the ninth day, at a stage immediately after closure of the brain has been effected. The nerve appears at this stage as a pyriform ganglionic mass, the narrow end of which is in close contact with the dorsal surface of the brain, while the rest of the nerve lies close alongside the brain, extending about half way down its side. By the tenth day the roof of the hind-brain has widened very greatly, and the root of the fifth nerve is now attached to the junction of the thin roof and thickened side of the brain. Before the end of the tenth day, the nerve branches distally ; and by the twelfth day the ophthalmic, maxillary, and mandibular branches are of considerable length, and have courses and relations very similar to those of the same v nerves in a five-day chick embryo (cf. Fig. 115).

VII and VIII. The facial or seventh, and auditory or eighth cranial nerves are, as in the chick, very intimately connected, or actually continuous with each other, from their h'rst appearance. They can be recognised before the end of the ninth day ; and by the tenth day the facial nerve has acquired its definite relation to the hyoid arch, as in a five-day chick embryo (Fig. 115). The auditory nerve appears to be continuous with the epithelium of the auditory vesicle from its earliest appearance.

IX. The glosso-pharyngeal, or ninth cranial nerve, as in the chick, arises by multiple roots from the side of the medulla oblongata, immediately behind the auditory vesicle. Its main stem lies in the first branchial arch.

X. The pneumogastric, or vagus, or tenth cranial nerve has, in the rabbit embryo of the twelfth day, almost exactly the same course and relations as in a chick embryo of the fifth day (Fig. 115). It arises by a considerable number of roots from the side of the medulla oblongata, behind the roots of the glossopharyngeal nerve ; the most anterior of the roots of the pneumogastric nerve is, as in the chick, directly continuous with the posterior root of the glosso-pharyngeal nerve ; while the hindmost root of the pneumogastric is of great length, and runs backwards along the side of the medulla oblongata to the ganglion of the first spinal nerve, with which it is closely connected (cf. Fig. 115). The roots of origin of the pneumogastric nerve converge to form a single large trunk, which lies immediately behind the trunk of the glosso-pharyngeal nerve ; it expands to form a large oval ganglion, beyond which it divides into a small branch to the second branchial arch, and a much larger visceral branch which runs backwards to the heart, lungs, and stomach.

XI. The spinal accessory or eleventh cranial nerve. The development of this nerve has not yet been determined in the rabbit.

XII. The hypoglossal or twelfth cranial nerve. Exactly opposite the roots of the pneumogastric nerve in rabbit embryos of the twelfth day, but arising from the medulla oblongata at a more ventral level, and nearer the median plane, is a second set of nerve roots. These are quite as numerous as the more dorsally placed pneumogastric roots, but are more slender ; they converge, and unite to form the hypoglossal nerve. Anatomically, the roots of the pneumogastric and hypoglossal nerves, at this stage, have relations closely comparable to those between the dorsal and ventral roots of a spinal nerve ; but it is not yetclear whether this comparison has any morphological value. The roots of the hypoglossal nerve are probably correctly regarded as belonging to the same category as the ventral spinal roots, but their relations to the roots of the pneumogastric must be considered at present as much more doubtful.

The Spinal Nerves.

The earliest stages in the development of the spinal nerves have not yet been described in the rabbit. The dorsal roots and the ganglia are clearly established by the end of the ninth day ; the ventral roots develop later, apparently during the tenth day.

The ganglia of the dorsal roots are at first of very considerable width ; almost as wide, in fact, as the mesoblastic somites ; so that on the twelfth day there are hardly any intervals between the spinal nerves, the successive ganglia being practically in contact with one another along the greater part of the length of the spinal cord.

Beyond the ganglia the nerves narrow rapidly, and have the normal proportions. The main divisions of the spinal nerves are early established, and are all present by the eleventh day (Fig. 165) . The nerve trunk, beyond the ganglion, divides at once into a smaller dorsal branch, NN' ; and a larger ventral branch, NN ; each branch containing nerve fibres from both the dorsal and ventral roots of the nerve. The dorsal branch, NX', runs outwards and upwards, to the muscles and skin of the back ; while the ventral or larger branch, NN, runs downwards in the body wall, and in the somites opposite the limbs sends branches into these latter.

6. The Sympathetic Nervous System

This has received much attention, but several points concerning its earl}' origin still remain in doubt. Before the end of the eleventh day it is already well established (Fig. 165, NY), consisting of a main ganglionated cord running along each side of the body, close to the dorsal surface of the aorta, and receiving branches from the ventral branches of the several spinal nerves as it passes these. Dr. Paterson, from observations chiefly on rat embryos, but partly on rabbits, concludes that the longitudinal cord is the first part of the sympathetic system to be developed, that it arises in the mesoblast entirely independently of the spinal nerves, and is at first devoid of ganglia ; he believes that the connection of the longitudinal cord with the spinal nerves is a secondary one, and is effected by outgrowths from the ventral branches of the spinal nerves after the longitudinal cords are established. These observations are, however, so entirely at variance with what is known as to the development of the sympathetic nervous system in other Vertebrates, in which the sympathetic develops merely as a specialised portion of the spinal nervous system, that it seems preferable to suspend judgment on the matter, pending renewed investigations.

The connections of the spinal nerves with the longitudinal sympathetic cords are limited to the thoracic and lumbar regions, but the cords themselves extend forwards along the neck to the head, where they acquire connections with the hinder cranial nerves.

7. The Supra-renal Bodies

The supra-renal or adrenal bodies, which in the adult rabbit form a pair of small, round, yellow bodies, a little way in front of the kidneys, are developed from two distinct sources.


The outer or cortical portion of the supra-renal body is developed from a mass of mesoblast cells which appears about the twelfth day, lying in front of the kidney, and between the aorta and the root of the mesentery.

The medullary portion of the supra-renal body is formed from a column of cells, which grows out from the longitudinal sympathetic cord about the fifteenth day, and makes its way into the mesoblastic mass which gives rise to the cortical layer. This mode of development agrees with what is known as to the formation of the supra-renal bodies in other Vertebrates, but leaves the real morphological meaning of these curious structures still undecided.

The Development of the Sense Organs

1. The Nose

There is very little of special interest about the olfactory organ of the rabbit, which resembles in most features of its development that of the chick. A special diverticulum arises at an early stage from each olfactory sac, which acquires a separate opening into the mouth, through the naso-palatine canal, and becomes the organ of Jacobson.

2. The Eye

The general history of development of the eye of the rabbit is very similar to that of the chick ; the formation of the optic vesicles as outgrowths of the fore-brain, the doubling up of the vesicles to form the optic cups, the pitting-in of the surface epiblast to form the lens, and the subsequent fate of the several parts being essentially the same in the two cases. One of the most marked points of difference is the much smaller size of the eye in the rabbit (cf. Figs. 115 and 148).

The optic vesicles arise as lateral outgrowths of the forebrain, at a very early stage. Before the end of the ninth day, i.e. before the fore-brain is closed dorsally, the optic vesicles (Fig. 145) are already conspicuous structures. The vesicles soon become constricted at their origins from the fore-brain, the constricted portions giving rise to the optic stalks. As the constrictions proceed from above downwards, the optic stalks remain connected with the ventral surface or floor of the fore-brain (Fig. 155).

The optic cup. On the tenth day, the doubling up of the optic vesicle to form the optic cup commences, and by the fourteenth day (Fig. 155) it is completed. The process of doubling up takes place in very much the same way as in the chick ; and, although occurring simultaneously with the formation of the lens, it is to be ascribed rather to a complicated mode of growth on the part of the walls of the optic vesicle itself, than to mechanical inpushing by the developing lens.



FIG. 155. A transverse section across the head of a Rabbit Embryo of the fourteenth day, the section passing through the eyes, the fore-brain and the cerebral hemispheres, x 14.

AO, central artery of retina, arising from internal carotid artery. BD, fold of the inner wall of the cerebral hemisphere, which forms the hippocampus major. HI. corpus striatum. BS, lateral ventricle, or cavity of the cerebral hemisphere. BTJ, optic thalamus. FM, foramen of Monro, leading from the third ventricle to the lateral ventricle. OC, inner or retinal wall of optic cup. OD, outer or pifjiiii-nt wall of optic cup. OL, lens. OM, upper eyelid. OO, lower eyelid. VJ, jninilar vein. X. fold of the inner wall of the cerebral hemisphere, which forms the choroid plexus of the lateral ventricle. XD, blood-vessels of the choroid plexus.


A choroidal fissure is formed along the ventral surface of the optic cup, as in the chick ; the only important point of difference being that, in the rabbit embryo, the process of folding or doubling up is not confined to the optic cup itself, but extends a certain distance along the optic stalk towards the brain. The. consequence is that the part of the optic stalk near to the eye (Fig. 155) is not a simple tube with thick walls, but a tube deeply grooved along its under surface by folding of its walls.

This groove, being continuous with the choroidal fissure, leads into the cavity of the optic cup, i.e. of the globe of the eye ; and it is by running along this groove that the central artery of the retina, a branch of the internal carotid artery (Fig. 155, AO), gains admittance to the interior of the eye. This artery supplies the retina throughout life, and during the development of the eye supplies the vitreous body and the capsule of the lens as well.

Of the two walls of the optic cup, the distal or inner wall (Fig. 155. oc) is, from the first, much thicker than the proximal or outer wall, OD ; the difference being a very pronounced one by the fourteenth day. From the inner layer, OC, the entire thickness of the retina proper is developed, the rods and cones being processes from its outer surface, which do not appear until shortly before birth.

The outer and thinner wall of the optic cup, OD, becomes converted, as in Vertebrates generally, into the pigment layer of the retina ; a stratum of hexagonal cells, closely fitted together, with which the retinal rods ultimately acquire very close relations. In the cells of this layer, granules of pigment are deposited at an early stage ; and up to a late period of development the black colour of the eye is due to this layer, the choroid coat of the eye not developing, or acquiring pigment, until very near the time of birth (cf. Fig. 156).

Near the free edge of the optic cup, the two layers are ot approximately equal thickness (Fig. 156), and grow forwards in front of the lens to form the pigmented epithelium of the posterior surface of the iris.

The optic nerve. It is at present uncertain whether the fibres of the optic nerve of the rabbit are developed in situ, from the walls of the tubular optic stalk, or whether, as seems far more probable, they arise in the retina and grow inwards along the optic stalk to the brain. The nerve fibres from the two eyes cross one another in the floor of the third ventricle, to form the optic chiasma (Fig. 154, OT), and then continue their growth upwards and backwards, round the walls of the fore-brain, to the mid-brain.

The lens. During the tenth day the deeper part of the surface epiblast, opposite the optic vesicle, becomes thickened, forming the first rudiment of the lens. On the eleventh day this thickened patch becomes invaginated, forming the vesicle of the lens ; the mouth of the pit narrows, and by the end of the twelfth day or early on the thirteenth day it closes, completing the vesicle, which soon separates from the surface epiblast.

From the first, the inner or deeper wall of the lens vesicle is much thicker than the outer wall. The inner wall continues to increase in thickness, through elongation of the cells composing it, until by the end of the fourteenth day (Fig. 155, OL), the cavity of the vesicle is almost completely obliterated.

The lens continues to grow rapidly, and throughout the later stages of development is of large proportionate size. Its structure and relations on the twenty-first day are shown in Fig. 156, OL, where its inner surface is seen to be very strongly convex, and the outer surface less markedly so. The axial cells of the lens remain straight or nearly so, while the more marginal ones are curved in the direction indicated by the lines crossing the lens in the figure. The first formed part of the lens acts as a nucleus, round which successive layers of cells are added on in the later stages of development. These arise at the equator of the lens, and, increasing rapidly in length, spread on to the faces of the lens, over the ends of the first formed cells.

The lens, during the time of its formation, is invested by a sheath of mesoblast. According to Kolliker, this is present from the first as a thin layer, between the epiblastic thickening, which gives rise to the lens, and the optic vesicle ; and is carried in by the lens as this becomes invaginated. Most other investigators maintain that it arises from mesoblast which gains admittance into the globe of the eye through the choroidal fissure. This mesoblastic investment of the lens is very vascular, the blood being brought to it by a branch of the central artery of the retina (Fig. 155, AO). This divides into very numerous branches on the inner or deeper surface of the lens, which extend round its margin and cover the outer surface as well. There are no veins which correspond exactly to this artery, the blood being returned by veins in connection with the iris. This vascular investment to the lens is merely a provisional structure, serving for its nutrition during growth ; it disappears completely when the lens has reached its full she.




FIG. 156. A transverse section across the head of a Eabbit Embryo of the twenty-first day, the section passing through the centres of the eyes (ef. Figs. 149 and 151). x 8.

BE, orbito-sphenoidal cartilage. BY, olfactory lobe. CC, cornea. DA, suborbital gland. DB, submaxillary gland. DC, duct of submaxillary gland. DE, hair follicles. ET, pre-sphenoidal cartilage. FA, frontal bone. HB," basihyal cartilage. MB, mandible. MC, Meckel's cartilage. OB, buccal cavity. OC, inner or retinal layer of optic cup. OD, outer or pigment layer of optic cup. OG-, iris. OL, lens. OM, upper eyelid. OO, lower eyelid. PF, posterior narial passage. PI, palatine bone. TE, deciduous grinding tooth of upper jaw. TF, permanent grinding tooth of upper jaw. TG, deciduous grinding tooth of lower jaw. TK, permanent grinding tooth of lower jaw. TM, tooth papilla. TN, tongue. TT, enamel organ. ZO, zygoma. V, mandibular branch of trigemiiial nerve.


The vitreous body is derived from the mesoblast which grows into the cavity of the optic cup, through the choroidal fissure. It is extremely vascular in the early stages of its formation, receiving its blood from the central artery of the retina. . There is no structure in the rabbit corresponding to the pecten of the bird.

The cornea (Fig. 156, cc) is formed, as in the chick, from mesoblast, which spreads in between the surface epiblast and the lens ; and the anterior chamber of the eye is a space which appears at a rather late stage, between the cornea and the lens.

The choroid and sclerotic are formed, as in the chick, from the mesoblast surrounding the optic cup. They are developed very late; and on the twenty-first day (Fig. 156), when the cornea is well developed, the choroid and sclerotic are merely represented by a thin layer of connective tissue, devoid of pigment. The sclerotic of the rabbit is not cartilaginous at any stage.

The eyelids are folds of skin, above and below the eyeball." They appear early, and by the fourteenth day have attained some size (Fig. 155, OM, oo). By the nineteenth or twentieth day they have grown completely over the eye, and meet each other along their free edges (cf. Fig. 149) ; a little later (Fig. 156, OM, oo) the edges of the two eyelids fuse together, the epidermal layers becoming continuous with each other ; this fusion persists throughout the remaining period of development, and is the cause of the blindness characteristic of the young at birth.

The third eyelid, or nictitating membrane, is a similar fold of skin, arising at the inner angle of the eye, and lying between the other two eyelids and the eyeball.

The lacrymal glands arise as solid ingrowths of epiblast into the underlying connective tissue, which subsequently become hollowed out to form the cavities of the glands and ducts.


3. The Ear

The ear of the rabbit, like that of the chick, is derived from a pitting-in of the epiblast at the side of the hind-brain. By closure of its mouth, the pit becomes a vesicle or sac, imbedded in the mesoblast of the side of the head ; and from the walls of this sac, which are of epiblastic origin, the epithelial lining of the vestibule and of its various prolongations is derived ; the semicircular canals, cochlea, and other parts being formed by outgrowths or constrictions of the originally simple sac.

The mesoblast immediately surrounding the sac gives rise to the connective tissue wall of the auditory labyrinth, while the mesoblast a little distance off gives origin to the cartilaginous auditory capsule (cf. Fig. 159). Between the labyrinth and the cartilaginous capsule a series of lymphatic spaces appear, filled with fluid, in which the labyrinth hangs suspended. Finally, important series of accessory organs, characteristic of air-breathing Vertebrates the tympanic membrane, Eustachian tube, auditory meatus, auditory ossicles, and external ear are formed, and acquire definite relations with the essential organ of hearing, i.e. the auditory vesicle itself.

The auditory vesicles arise in the rabbit, towards the end of the ninth day, as a pair of shallow depressions of the epiblast at the sides of the hind-brain. During the tenth day each pit deepens rapidly, and by the end of the day the mouth of the pit narrows and closes, converting the pit into the closed auditory sac or vesicle (Fig. 147, EI), which lies imbedded in the side wall of the head, opposite the first branchial arch.

The auditory vesicle is at first spherical, but soon becomes triangular in outline as seen in transverse sections. The dorsal angle of the triangle, which marks the place where the vesicle separates from the external epiblast, grows upwards as a long tubular process, the recessus vestibuli (Fig. 158, ER), which follows the curvature of the brain wall, and ends blindly at its dorsal extremity.

From the outer side of the vestibule, a wide lateral diverticulum arises, from which the semicircular canals are developed at a slightly later stage (Fig. 158, ED, EH). The ventral angle of the vestibule is prolonged downwards and inwards as a curved finger-like process, the cochlear canal (Fig. 158, EL).


The auditory nerve (Fig. 158, vin) develops very early, as already noticed, and by the tenth day, if not indeed from its earliest appearance, is intimately connected with the inner wall of the vestibular sac.



FIG. 157. A diagrammatic section across the head of an adult Rabbit, to show the relations of the internal ear, tympanic cavity and membrane, and the auditory ossicles. The section is drawn as seen from the front, and is taken along a line joining the reference letters so and MN in Fig. 1C2 (p. 405). The external ears are cut short, close to their bases, and the floccular lobes of the cerebellum, which lie between the three semicircular canals of each side, are omitted entirely. (From Marshall and Hurst.)

B, buccal cavity. BO, basi-occipital. C, cochlea. CA, right external carotid artery. CE, cerebellum. E, external ear or pinna. EM, external auditory meants. ET, Eustaohian tube. H, body of the hyoid. LA, right lingual artery. M. malleus ; to its inner side are seen the incus and stapes. MN", mandible. MO, medulla oblougata. N, posterior nasal chamber. P, soft palate. PO, periotic. S, post-tympanic proee-.of squamosal. SC. anterior vertical semicircular canal. SO, supra-occipital. T, tympanic bone. TC. tympanic cavity. TM, tympanic membrane.


The condition on the fifteenth day is shown in Fig. 159, the section, on the left side, being taken at a level slightly anterior to that of the right side. The recessus vestibuli, ER, is still large, and is dilated at its upper end in a club-shaped manner. The three semicircular canals are well established: they are formed, as in the chick and frog, from flattened saccular out growths of the auditory vesicle, the two walls of each outgrowth coming in contact and fusing, so as to form a curved tube opening into the vestibule at both ends. The section (Fig. 159) passes through the stem common to the two vertical semicircular canals, ED, and also through the horizontal canal, EH. Each semicircular canal has already acquired an ampulla at one end.



FIG. 158. A transverse section across the head of a Rabbit Embryo at the end of the eleventh day, the section passing through the medulla oblongata, the ears, and the pharynx. The plane of section of the right half of the figure is slightly anterior to that of the left half. (Compare Fig. 147.) x30.

CH, notoclionl. EB, membrane closing hyomandibular cleft. ED, common stem of the two vertical semicircular canals. EH, rudiment of the external or horizontal semicircular canal. EL, cochlear canal. EK, recessus vestibuli. EV, auditory vesicle. HM. hyomandilmlar pouch. TP, pharynx. VF, fourth ventricle. VJ, jugular vein. VIII, auditory nerve.


The body of the vestibule is partially divided by a constriction into a larger division, the utriculus, with which the semicircular canals are connected ; and a smaller division, the sacculus, which opens through a narrow neck, the canalis reuniens, into the cpchlear canal, EL. This latter is a tube of fairly uniform diameter, curved as shown in the figure, and with its wall markedly thicker along the inner than the outer side of the curve. A cartilaginous periotic capsule, EC, is present, surrounding the ear, but at some little distance from it ; the recessus vestibuli alone projecting beyond the capsule.


FIG. 159. A transverse section across the head of a Rabbit Embryo of the fifteenth day, passing through the medulla oblongata, the ears, and the pharynx. The plane of section of the left side of the figure is slightly anterior to that of the right side, x 16.

A.C. carotid Bltcry, giving <jfl a small branch which runs through the arch of the stapes. CH. notochord. EB, tympanic membrane. EC, cartilaginous auditory capsule. ED, common stem of the two vertical semicircular canal?. EH, external or horizontal .semicircular canal. EL, cochlear canal. EO, external auditory meatus.


At a stage a little later than that shcw r n in Fig. 159, the cochlear canal, which up to this point has been only slightly curved, begins to form the spiral turns, so characteristic of the adult (Fig. 157, c), the twisting being brought about by growth in a spiral manner of the blind end of the canal.

The cochlear canal becomes the scala media of the cochlea in the adult. Immediately outside it the mesoblast becomes excavated to form a couple of tubular passages, the scala vestibuli and scala tympani, which lie respectively above and below the scala media or cochlear canal. The scala vestibuli and scala tympani commence at the basal end of the cochlea, and gradually extend along it towards its apex, following the turns of the spiral ; and ultimately, on reaching the apex, they open into each other, though not until a very late stage of development. From the epithelium of the floor of the cochlear canal, or basilar membrane, the organ of Corti is developed ; while the roof of the cochlear canal, separating it from the scala vestibuli, is spoken of in the adult as the membrane of Reissner.

At the base of the cochlea, the scala vestibuli opens into the peri-lymphatic space surrounding the central part of the vestibule, while the scala tympani is closed at its base by the membrane of the fenestra rotunda.

Similar peri-lymphatic passages are formed, by excavation of the mesoblast, around the semicircular canals.

As in the frog, there is at first a single patch of the epithelium of the auditory vesicle with which the auditory nerve is continuous. This single, large patch becomes ultimately broken up into several smaller ones, which by growth of the intervening strips of epithelium are separated further and further from one another until they reach their adult positions.

The accessory auditory apparatus of the rabbit is, in a general way, similar to that of the frog or the chick, but is more complicated.

The Eustachian tube (Fig. 157, ET) is formed from the hyomandibular gill-pouch. This reaches very close to the surface in the early stages of development, but does not open to the exterior at any period. On the eleventh day (Fig. 158, HM) the hyomandibular pouch reaches almost to the surface, the hypoblast of the pouch meeting the epiblast at the bottom of the external groove, so that the cleft is at this stage closed only by a very thin branchial membrane, EB, formed of epiblastic and hypoblastic layers without any intervening uiesoblast. As shown in the figure, the hyomandibular pouch lies at this stage some distance ventral to the ear, and the two structures are completely independent of each other.

By the fifteenth day (Fig. 159) the conditions have changed materially. A thick layer of mesoblast has grown in between the epiblast and hypoblast of the branchial membrane, so that the hyomandibular pouch is now separated from the surface of the head by a thick plate, EB, which becomes later on the tympanic membrane. Further, by growth upwards of its lips, and through the general thickening of the side walls of the head, the shallow hyomandibular groove of the earlier stage is converted into a deep pit, EO, the external auditory meatus, the margin of which is already commencing to grow out as the rudiment of the pinna or external ear (cf. Figs. 149 and 157).

In the later stages (cf. Fig. 157), the external meatus, EM, becomes much longer, and the pinna attains enormous dimensions ; the tympanic membrane, TM, becomes relatively much thinner than at the fifteenth day ; while the Eustachian passage becomes more distinctly tubular, and, owing to the formation of the palate, P, now opens into the posterior narial chamber instead of directly into the buccal cavity.

With regard to the auditory ossicles of the rabbit, it is difficult to speak with certainty. The stapes (Fig. 159, SA) forms, about the fifteenth day, as a ring of cartilage, which from its first appearance is in close connection with the outer wall of the periotic capsule, and apparently continuous with this, at the place where the fenestra ovalis is formed a little later. The ring-like form of the stapes is apparently due, as shown in Fig. 159, to its being formed around a small branch of the carotid artery, AC.

Concerning the origin of the other two auditory ossicles of the mammal, the malleus and incus (Figs. 157, M, and 159, MA), there has been much discussion. While it appears very probable that they are formed in connection with the cartilaginous bars of one or more of the visceral arches, investigators differ widely as to whether both are developed from the mandibular bar, which is perhaps the most generally accepted view, or both from the hyoidean bar, or one from each of these bars. There are, at present, no recorded observations which determine the matter satisfactorily in the case of the rabbit.

The malleus can be recognised on the fifteenth day (Fig. 159, MA) ; it is, from its first appearance, imbedded in the substance of the tympanic membrane, EB, and is for some time continuous with the posterior end of the mandibular bar, or Meckel's cartilage.


The Development of the Digestive System

A. The Alimentary Canal

1. General Account

The general history of the development of the alimentary canal of the rabbit is closely similar to that of the chick. The greater part of the length of the canal is formed from the mesenteron, which, as in the chick, is a tubular cavity included within the embryo by the process of constriction, through which the embryo becomes separated from the yolk-sac (cf. Figs. 146 and 147). Owing to this mode of formation of the mesenteron, it necessarily communicates with the cavity of the yolk-sac in the early stages, and so long as the yolk-stalk remains tubular. The mesenteron may, therefore, as in the chick, be divided into three lengths : fore-gut, mid-gut, and hind-gut ; the fore-gut (Figs. 146 and 147, GF) being the anterior portion, in which roof, sides, and floor are all alike present ; the hind-gut, GH, being the similar portion at the hinder end of the body ; and the mid-gut, GT, being the median portion, which opens through the yolk-stalk into the cavity of the yolk-sac, and which consequently has no floor. Fore-gut and hind-gut increase in length, at the expense of the mid-gut, as the embryo becomes more and more sharply constricted from the yolk-sac ; and ultimately, when the yolk-stalk becomes solid, about the thirteenth day, the mid-gut as a separate division of the alimentary canal ceases to exist (cf. Figs. 146, 147, and 150).

The mouth and anal openings are formed, as in other Vertebrates, by stomatodgeal and proctoda3al invaginations of the epiblast at the anterior and posterior ends of the embryo respectively, which meet and open into the mesenteron, and so place it in communication with the exterior.

The alimentary canal is at first straight, or merely follows the curvature of the body, and is situated immediately ventral to the notochord. It remains in this condition, throughout life, in the pharyngeal and cesophageal regions, and also at its extreme hinder end ; but along the rest of its extent it shifts ventral wards, remaining connected with the dorsal wall of the body cavity by a mesentery (Fig. 165, MH). In the region of the small intestine the alimentary canal increases in length far more rapidly than the body of the embryo, and becomes in consequence thrown into folds, in order that it may be accommodated within the body cavity.

2. The Stomatodaeum

The relations of the stomatodasal pit are practically the same as in the chick. Perforation of the stomatoda3al membrane is effected at an early stage, before the end of the tenth day. The pituitary body arises, still earlier, as a diverticulum from the posterior and dorsal angle of the stomatodasal pit ; its further development has already been described in the section dealing with the formation of the brain (p. 376).

3. The Buccal Cavity and Pharynx

The pharyngeal region of the mesenteron is, from the first, distinguished by its great width (Figs. 158 and 159, TP). Early on the tenth day, the branchial pouches arise as paired diverticula from the sides of the pharynx ; and, opposite to the outer ends of the branchial pouches, branchial grooves are formed on the surface of the neck, marking out the boundaries of the several visceral arches. The walls of the branchial pouches and of the corresponding branchial grooves come into close contact, a thin branchial membrane (Fig. 158, EB), consisting of epiblast and hypoblast, without any intervening mesoblast, alone separating the two. This membrane, however, remains intact ; and in the rabbit none of the gill-clefts are ever completely formed, or open to the exterior at any stage of development. There are also no traces of gills, either external or internal, at any period in the rabbit.

The visceral arches are well developed, and on the twelfth day (Fig. 161) the maxillary. MX, mandibular, MX, hyoid, HY. and first branchial arches form conspicuous ridge-like projections in the side walls of the pharyngeal region. Of the branchial grooves, or external depressions separating the successive arches, the hyomandibular groove, HM, is by far the most conspicuous. The further development of the hyomandibular groove, and the mode in which it gives rise to the external auditory meatus, have already been described in the section dealing with the ear (p. 397). The tongue is developed as a swelling in the floor of the buccal cavity ; it commences to form on the twelfth or thirteenth day, and by the eighteenth day (Fig. 151, TN) has attained the form characteristic of the adult.


FlG. 161. A Rabbit Embryo at the end of the twelfth day, seen from the right side. The yolk- stalk and allantoic stalk are cut short, close to the body of the embryo, x 9.

BL, cerebellum. BM. mid-brain. BB..1, first branchial arcli. El, auditory vesicle. HM, hyomandibular groove. HY, hyoid arch. LA, fore limb. LP, hind limb. MN, mandibular arch. MS, mesoblastic somite or protovertebra. MX, maxillary arch. OC, eye. OF, olfactory pit. TA, allantoic stalk, cut short. TL, tail. Vi 1 , fourth ventricle of brain. YS,' yolk-stalk, cut short.


The boundary line between stomatodasum and mesenteron is impossible to fix absolutely, in the later stages of development ; but its position may be approximately determined, if it be remembered that the stalk of the pituitary body (Fig. 151, PT) marks the posterior boundary of the stomatodasum in the middorsal line ; while, on the floor of the buccal cavity, the boundary line lies in front of the root of the tongue ; the whole of the tongue being formed from the mesenteron, and being therefore covered with hypoblastic epithelium.

The palate is formed, about the fifteenth day, by a pair of horizontal ridges which grow inwards from the sides of the buccal cavity, and, meeting each other in the median plane, fuse to form a horizontal shelf (Fig. 151, PL), which separates the nasal chamber above from the buccal cavity below. The fusion of the two halves of the palate proceeds from before backwards ; and the palate ends with a free posterior edge, behind which the nasal and buccal chambers are continuous with each other (Fig. 151, TP).

4. The Oesophagus

The hinder end of the pharynx narrows very rapidly, and passes abruptly into the straight tubular oesophagus (Figs. 150, and 151, TO). It has not yet been determined whether the oesophagus of the rabbit, like that of the chick and tadpole, passes through a stage in which it is solid for a time.

5. The Stomach and Intestine

The stomach becomes evident, as a distinct dilatation of the alimentary canal, about the thirteenth day ; its long axis at first -corresponds with that of the body, but later on it shifts its position, and becomes placed at first obliquely, and then almost directly across the body.

The intestine undergoes changes corresponding fairly closely with those already described for the chick. The lengthening of the intestine is effected almost entirely in two situations, giving rise to two ventrally directed loops. Of these, the proximal or duodenal loop is formed immediately behind the stomach, and in the rabbit attains a considerable length (Fig. 160, E). The distal or vitelline loop is formed by elongation of the > -shaped loop of the intestine already present on the twelfth day, and from the apex of which the yolk-stalk, YK, arises ; the vitelline loop attains an enormous length in the rabbit.

A short length of the intestine, between the duodenal and vitelline loops, remains in the rabbit, as in the chick, stationary throughout the whole period of development ; it is attached to the dorsal wall of the body cavity by a very short mesenterial fold, and is easily recognised in an adult rabbit.

A well-developed post-anal gut, or prolongation of the hinder end of the intestine into the tail, is present on the tenth and eleventh days. By the twelfth day (Fig. 150), the greater part of this has already disappeared ; a small diverticulum of the cloacal cavity, GP, marks its basal portion, and detached fragments of it may persist for a tinie at intervals along the tail.

This post-anal gut is probably a secondary feature, and due, as in the frog, to the drawing out of the alimentary canal into the tail as this latter lengthens.

6. The Proctodseum

The proctodfcum in the rabbit is little more than the actual anal opening ; it develops late, and is usually not formed until about the sixteenth day.

B. Organs Developed in connection with the Alimentary Canal

1. The Teeth

Teeth are cutaneous structures, developed from the mucous membrane covering the jaws. They appear in rabbit embryos during the third week, and are at first independent of the bones of the jaws ; indeed, the upper teeth develop before the maxillary bones are formed (cf. Fig. 15G). The jawbones, however, soon acquire close relations with the teeth, growing round them, and inclosing them in sockets.

In the rabbit, as in Mammals generally, there are two sets of teeth, known as milk or deciduous, and adult or permanent, respectively. The deciduous dentition of the rabbit is represented by the formula : di. - ; dc. - ; dm. - ; the corresponding formula for the permanent dentition being,

.20 3 3

i. p c. -, pm. 2 , m. -.

The milk, or deciduous, teeth in the rabbit are lost very early. The deciduous incisors, corresponding to the large chisel-shaped incisors of the permanent set, are very small, and are shed before the birth of the young rabbit. The second pair of deciduous incisors of the upper jaw are much larger, and persist as functional teeth for about three weeks after birth, lying wedged in between the large and small permanent incisors. For the first three weeks after birth there are therefore three upper incisors on each side in the rabbit ; the first and third being the permanent incisors, and the middle one being the deciduous second incisor, which has not yet been shed. The deciduous molars (Fig. 156, TF, TG) are of considerable size, and persist until three or four weeks after birth, when they are pushed out by the permanent premolars developed beneath them.


FIG. 162. The skull of the Eabbit, from the right side. The middle portion of the zygomatic arch and Ihe right half of the mandible have been removed. (From Marshall and Hurst.)

A, external pterygoid process of ali-sphenoi<l. AS, Hli-sphonoid. B, internal orbital foramen. BO, basi-occipital. B8, bad-sphenoid. C, occipital condyle. D, mandibnlur symphysis. EO, ex-occipital. F, frontal. FA, foramen lacenim anterius. FM, foramen lacerum medium. Gr, orbital groove, for oplitlialraic division of trigeininal nerve. I, anterior upper incisor. IF, infra-orbital foramen. IP, inter-parietal. J, lower incisor. L, lacrytnal bone. LF, lacrymal foramen. M, maxilla. MN", mandible. M". nasal bone. OF, optic foramen. 'OS, orbito-sphenoid. f, parietal. PE, paroccipital process of ex-occipital. PL, palatine bone. PM, pro-maxilla. PO, periotic. PT, pterygoid. S. sqnamosiil. SF. stylo-mast oid foramen. SO, supra-occipital. T, tympanic bone. ZM, zygomatic process of maxilla, cut short. ZS, xygomatic process of squamosal, cut short.


A fully formed tooth consists chiefly of dentine, covered on its crown, or grinding surface, with a cap of a very hard and densely calcified substance, the enamel ; and invested, especially round its deeper part or root, by a layer of bony substance, the cement. The dentine is hollowed out by the pulp cavity, in which are lodged the blood-vessels and nerves of the tooth.


These gain admittance through a larger or smaller hole in the root, or fang, of the tooth ; the hole remaining widely open throughout life in the rabbit, and other animals in which the teeth grow continuously throughout life, but becoming reduced to one or more very small apertures in the majority of Mammals, in which the teeth cease growing after they have reached their full size.

Teeth, as already noticed, are cutaneous structures; and of the substances of which the tooth consists, the enamel is formed from the epithelium, and the dentine and cement from the underlying connective tissue layer or dermis.

The first step in the formation of a tooth consists in an ingrowth from the deeper layer of the epithelium into the connective tissue of the gum (cf. Fig. 156). This ingrowth soon becomes hollow and flask-shaped, its deeper end dilating into a sac (Fig. 156, TT), while its superficial part forms a narrow solid neck or stalk, which remains in connection with the surface epithelium. Opposite the deeper end of the flask, the connective tissue of the gum becomes condensed to form the dental papilla (Fig. 156, TM). The deeper end of the epithelial flask, or enamel organ as it is called (Fig. 156, TT), now becomes closely applied to the dental papilla, which gradually acquires the definite shape of the crown of the tooth to which it is going to give rise.

The enamel organ (Fig. 156. TT), at this stage, is a flattened sac, consisting of outer and inner epithelial layers, and having its cavity occupied by a reticulum of stellate cells ; the outer epithelial layer is still connected with the surface epithelium by a narrow stalk or string of cells, while the inner layer forms a cap, closely embracing the top and sides of the dental papilla.

This cap consists of a single layer of very regularly arranged, six-sided, columnar epithelial cells ; and it is by calcification of the substance of these cells that the enamel layer of the tooth is produced. Calcification commences at the surface of the enamel organ next to the dental papilla, and gradually spreads outwards through the cells of the enamel organ.

The dentine is formed by calcification of the dental papilla, and is therefore of mesoblastic origin. Calcification appears first at the surface of the papilla next to the enamel organ, so that the crown of the tooth is the first part to be formed ; and, when once completed, no further change in the shape of the crown can occur.

The mode of formation of the dentine is as follows. The cells at the surface of the dental papilla form a single layer of finely granular nucleated cells, closely arranged side by side, and spoken of as odontoblasts. The most superficial parts of the odontoblasts become converted into, or else form by excretion, a gelatinous matrix in which calcification soon occurs, forming the dentine. The deeper parts of the odontoblasts, containing the nuclei, remain soft and unaltered ; they give off fine processes towards the surface of the tooth, which lie in channels in the dentine, these channels being the dentinal tubules of the adult. By a continuance of this process the dentine increases in thickness ; the odontoblasts, which are the active agents in the process, forming a layer on the inner surface of the dentine, and sending out fine radial prolongations into the dentinal matrix.

The follicle, or tooth-sac, is formed by a condensation of the vascular mesoblast around the tooth. The cement is a thin layer of bone formed round the tooth by the wall of the follicle, which acts as the periosteal membrane.

The permanent teeth are formed in the same way as the deciduous teeth ; their enamel organs arising as outgrowths from the necks of those of the deciduous teeth (Fig. 156).

2. The Thyroid Body

The thyroid body of the rabbit arises early in the tenth day, as a median thickening of the epithelium of the floor of the pharynx, which grows downwards into the connective tissue immediately in front of the pericardial cavity. The stalk of connection with the pharyngeal floor narrows, and during the eleventh day disappears, leaving the thyroid as a solid epithelial body (Fig. 150, TH) embedded in the mesoblast of the floor of the pharynx, immediately in front of the truncus arteriosus, and between the roots of the carotid arches.

In the later stages the thyroid body widens transversely, giving off two lateral lobes which rapidly increase in size. A cavity appears in the median portion, and soon extends into the lateral lobes, from which outgrowths, some hollow and some solid, soon arise. As the heart shifts backwards into the thorax, the thyroid body also moves its position, coming into close relation with the upper rings of the trachea.

3. The Thymus

The thymus of the rabbit is formed by bud-like outgrowths from the epithelium of one of the hinder branchial pouches. These buds first become conspicuous about the fourteenth day ; they soon separate from the walls of the pharynx, and gradually shift backwards, increasing greatly in size as they do so, until they reach their final position at the anterior end of the thorax.

4. The Lungs

The lungs arise in the rabbit, much as in the chick or frog, from the ventral wall of the mesenteron, at the place where it narrows, immediately behind the pharyngeal region, to form the oesophagus.

On the tenth day the cavity of the oesophagus, which is elsewhere circular in transverse section, becomes laterally compressed at its anterior end, immediately behind the pharyngeal region. By the outgrowth of two horizontal ridges from its side walls, which meet and unite in the median plane, a short length of the oesophagus becomes divided into two tubes : of these, the dorsal tube is the oesophagus itself; while the ventral one, or laryngeal chamber, is a short tube, ending blindly behind . but opening in front into the oesophagus through the orifice which afterwards becomes the glottis (cf. Fig. 150).

From the laryngeal chamber the lungs arise, on the eleventh day, as a pair of lateral diverticula, which grow backwards along the dorsal pai't of the body cavity and the sides of the oesophagus (Fig. 150, LG).

The lungs, being thus formed as outgrowths from the alimentary canal, will, like the canal itself, have mesoblastic walls, lined by a hypoblastic epithelium.

On the twelfth day secondary outgrowths arise from the main tube or bronchus of each lung, and these in the later stages branch freely to form the smaller bronchi, from the terminal branches of which the air cells are formed about the time of birth.

The branchings of the bronchi occur almost entirely towards the dorsal and outer surfaces of the lungs (Fig. 1G3), so that the original or main bronchial tubes, LB, lie close to the inner surfaces of the lungs. The smaller bronchi divide, for the most part, in a regular, dichotomous manner, as shown on the right-hand side of Fig. 1G3. The branching at first affects the hypoblastic lining alone, but about the thirteenth or fourteenth day (Fig, 1G3) the mesoblastic wall becomes divided by external grooves or clefts, which mark out the boundaries of the main lobes of the lungs. The trachea, or median part of the air passage, is at first very short ; but, as the neck elongates, and the lungs get carried back into the thorax, the trachea rapidly increases in length, and by the eighteenth day (cf. Fig. 151) the proportions are not very unlike those of the adult. The glottis, LT, at this stage is a longitudinal slit-like opening in the ventral wall of the oesophagus ; it is overhung by the epiglottis (cf. Fig. 150, LE), a fold at the back of the pharynx, marked off from the tongue by a well-marked transverse groove. The glottis leads into a dilated laryngeal chamber (Fig. 151), which is continued down the neck as the trachea, LR. The thyroid, CT, cricoid, and tracheal cartilaginous rings are already present, and have the same relations as in the adult.



FlG. 163. A transverse section across the thorax of a Rabbit Embryo of the sixteenth day. x 15.

A, dorsal aorta. CH, notoolionl. CP, pericanlial cavity. CR, pleural cavity. FN. neural arch of vertebra. LB, bronclius. LGr, luntr. NS. spinal cord. NY, sympathetic nerve cord. RA. right auricle. KB, left auricle. RD. inter-auricular >r|itum. HI. rib. RN. capituluiu of rib. RO. tubercle of rib. RV. right ventricle. RY, left ventricle. ST, ventral end of rib, from which the sternum is formed. TO, oesophagus. VD, left anterior vena cava. VI, posterior vena cava.



5. The Liver

The liver of the rabbit, like so many other important oi'gans, commences on the tenth day, arising as a diverticulum from the ventral surface of the mesenteron, about the junction of the stomach and duodenum. This diverticulum, which becomes the left bile duct of the adult, is directed ventral wards, and its blind end is in close relation with a thickened mass of condensed mesoblast which forms part of the ventral body-wall of the embryo, behind the heart, and in front of the yolk-stalk.

On the eleventh day, the right bile duct arises as an outgrowth from the left duct, close to its opening into the duodenum. From the lining epithelium of both right and left ducts, solid rods of hypoblast cells, the hepatic cylinders, grow out into the mass of condensed mesoblast around them. The hepatic cylinders branch and anastomose freely, forming a reticulum, the meshes of which are occupied by the connective tissue, in which blood-vessels early appear in large numbers.

By a series of further changes, which have not yet been accurately determined in the rabbit, the adult liver is formed. The cells of the reticulum become the hepatic cells, which are thus of hypoblastic origin ; while some at least of the cylindrical rods become hollow, and form the bile passages, which communicate directly or indirectly with the bile ducts (cf. Fig. 150, w).

The gall bladder arises on the eleventh day, as a diverticulum form the right bile duct.

The relations of the blood-vessels to the liver are much the same as in the chick, and will be described more fully in the section dealing with the development of the vascular system. It may be noticed here that in its early stages the liver has, as in the chick, especially close relations with the vitelline veins, through which the blood is returned to the embryo from the yolk-sac.

From the twelfth day onwards, the common part of the bile duct, where the right and left bile ducts join to enter the duodenum, lengthens rapidly, thus giving rise to the single bile duct of the adult rabbit (c/. Fig. 160, H).

6. The Pancreas

The pancreas arises, on the twelfth day, as a swelling or bulging of the dorsal wall of the intestine, slightly further back than the bile duct, and opposite the yolk-stalk. On the eleventh day it becomes much more sharply defined, and constricted off from the gut as a somewhat pyriform, hollow sac, which opens into the dorsal wall of the intestine, and gives off small buds from its surface. In the succeeding days these buds enlarge, and give off other similar buds from their sides, and so form a compound gland of the racemose type. The pancreas, therefore, in its mode of development agrees closely with the salivary or other ordinary glands, and differs markedly from the liver.

As the alimentary canal is at first straight, and lies but a little distance ventral to the notochord (Fig. 150), the pancreas, in its early stages, is embedded in the dorsal wall of the body cavity, and wedged in between the intestine and the dorsal aorta. As the intestine lengthens, to form the duodenal loop, the pancreas is drawn down with the mesentery, between the two limbs of the loop, and so attains its adult position (Fig. 160, F).

7. The Cloaca

On the twelfth day (Fig. 150), the rectum opens into a dilated cloacal chamber, TC, from which the stalk of the allantois, TA, opens, and into which the Wolffiaii ducts, KC, and ureters, KD, discharge. This cloacal dilatation lies in a rounded cloacal papilla, which forms a well-marked projection on the ventral surface of the embryo, behind the allaiitoic and yolk stalks, and in front of the root of the tail (Fig. 150).

Just before entering the cloacal dilatation, the intestine makes a rather sharp bend ventralwards, the distinctness of which is slightly exaggerated in Fig. 150. Between the intestine and the cloacal dilatation, and separating the two structures from each other behind the point of opening of the Wolffian duct, is a septum of connective tissue, which is well seen in the figure, where it is crossed by the reference line, TC.

During the next three days this septum extends backwards, its growth being effected by the union, in the median plane, of two lateral ridges to form a median partition. This partition divides the cloacal chamber into two separate portions, a dorsal or rectal chamber, and a ventral or urino-genital chamber. The proctodroal opening is established by this time, and the partition, on reaching the surface, divides this opening into separate anal and urino-genital apertures, the partition itself forming the perina3um, or transverse septum between the two apertures.

The anal opening lies on the posterior surface of the cloacal papilla, almost in the angle between the papilla and the tail, so that the cloacal papilla is from this time concerned with the urino-genital organs alone. The cloacal, or genital papilla as it may now be termed, elongates considerably, and the urino-genital aperture is prolonged as a median groove along its dorsal or posterior surface. From this stage, development differs in the two sexes : in the male the two lips of the groove unite to form the penial urethra, the papilla itself becoming the coqjus spongiosum of the penis. In the female the groove remains open, its borders forming the lips of the vulva.


Development of the Heart and Bloodvessels

The general relations of the heart and its various cavities, and of the great arterial and venous trunks, and the changes which they undergo during development, are much the same in the rabbit as in the chick, and it will not be necessary to describe them in detail in this chapter. The changes in the heart itself, and especially the mode of formation of the septa, by which the several cavities are shut off one another, will require closer consideration.

Besides the vessels of the embryo itself, there are two extraembryonic vascular systems : (i) the vitelline, or yolk-sac circulation, which is comparatively unimportant in the rabbit ; and (ii) the allantoic or placental circulation, which is of the utmost importance, as it affords the means through which the embryo receives its supply of nutriment from the mother, and is enabled to effect the necessary respiratory and excretory interchanges.

The vitelline circulation will be dealt with in the present section ; the relations of the allantoic vessels in the placenta will be treated separately, in the concluding section of this chapter.

1. The Heart

The heart of the rabbit, like that of the chick, is formed by the union of the two vitelline veins, which return to the embryo the blood from the vascular area.

The vitelline veins are formed in the mesoblast of the splanchnopleure, and appear at an early stage of development, when the folding-off of the embryo from the yolk-sac, by the side folds, has only just commenced. The right and left vitelline veins, and consequently the two halves of the heart as well, are therefore at first a considerable distance apart ; and in rabbit embryos of the ninth day (Fig. 145, R) they appear as a pair of tubes, lying along the sides of the head, opposite the hind-brain.

As the side-folds deepen, constricting off the embryo from the yolk-sac, the two tubes get carried round to the ventral surface of the embryo, where they lie close together, side by side. About the middle of the tenth day they fuse together to form a single tubular heart, lying in the floor of the pharyngeal region of the mesenteron, and having relations very similar to those of the heart in a chick embryo of about the thirtieth hour.

In the latter part of the tenth day, the heart, while it remains attached to the floor of the pharynx at both its ends, becomes free in the middle portion of its length ; and, growing rapidly, hangs down into the body cavity as a loop, which soon becomes twisted on itself like a letter S, and partially divided by constrictions into chambers (Fig. 147, R). The hinder or proximal limb of the heart, which receives the great veins, is the sinus venosus ; the first loop of the S is the auricular portion ; the second loop is the ventricular portion ; and the distal or anterior limb is the truncus arteriosus, from which the aortic arches arise as right and left branches.

The later changes undergone by the heart are of very considerable interest, and have been described with great care by Born. It will be convenient to deal with the several cavities in order, beginning at the hinder or venous end of the heart.

The sinus venosus, on the tenth day, is a vessel running transversely across the body, and slightly enlarged at its two ends to form the right and left corn.ua or horns. Each horn receives three veins: (i) the C u vie rian vein, which is formed by the junction of the anterior and posterior cardinal veins, returning venous blood from the body of the embryo generally ; (ii) the vitelline vein, returning blood from the yolk-sac ; (iii) the allantoic vein, returning blood from the allantois. The sinus venosus is at this stage nearly symmetrical, and opens into the auricular cavity by a wide median aperture.

By the eleventh or twelfth day, the right horn of the sinus venosus has become much larger than the left horn. The allantoic and vitelline veins, in place of opening separately into the sinus venosus, now unite before reaching the heart, and discharge into the sinus through a single vein, the posterior vena cava. The posterior vena cava and the right Cuvierian vein, or right anterior vena cava as it is now termed, open into the larger or right horn of the sinus venosus ; while the smaller left horn receives only the left Cuvierian vein, or left anterior vena cava. The opening from the sinus venosus into the auricle has now become more slit-like, and leads distinctly into the right half of the auricular chamber ; the slit-like opening is bounded by two valve-like folds of the endocardial lining of the heart, which may be termed the right and left venous valves respectively.

At a later stage the sinus venosus becomes absorbed into the right auricle, of which it now forms part ; the three ven.se cavse opening separately into the auricular cavity. Of the two venous valves, the left one disappears, while the right one becomes the Eustachian valve, by which the blood from the posterior vena cava, and for a time that from the right anterior vena cava as well, is directed into the left auricle.

The auricular portion of the heart. The originally single auricular chamber becomes divided into right and left auricles by a septum, which arises during the twelfth day from the dorsal wail of the auricular chamber, and grows down into its cavity (cf. Fig. 163, ED). For a time the lower and posterior edge of the auricular septum is free, but during the fourteenth day it meets and fuses with a cushion-like thickening of the margin of the auriculo-ventricular aperture.

Before this fusion is completed, however, a new aperture, the foramen ovale, is formed in the dorsal and anterior part of the auricular septum, through which free communication between the two auricles is maintained up to the time of birth of the young rabbit.

The pulmonary veins develop rather late, and are of small size until near the time of birth ; the two veins, from the right and left lungs respectively, unite to form a single vessel, which opens into the dorsal wall of the left auricle, very close to the auricular septum.

The ventricular portion of the heart. The ventricular cavity is at first single, and receives the blood from the auricular cavity through a transverse slit in its dorsal wall.

The division of the ventricular cavity into right and left ventricles is effected by a septum, which grows upwards from the apex of the ventricle towards the auriculo-ventricular aperture. This ventricular septum (cf. Fig. 163) appears about the twelfth day, and its position is indicated from an early period by a groove on the surface of the heart. The septum remains incomplete for some time, the two ventricles communicating above its free edge. About the fifteenth day the septum meets, and unites with, the cushion-like thickenings of the margin of the auriculo-ventricular aperture, and so completes the separation between the two ventricles.

The thickening of the wall of the ventricle is effected in the first instance, just as in the frog, by the ingrowth of muscular trabeculas into the cavity, which unite to form a reticulum (cf. Fig. 163), the proper wall of the ventricle remaining thin. In the later stages, however, the outer walls of the ventricles thicken considerably throughout their entire substance. Up to the time of birth there is practically no difference in thickness between the walls of the right and left ventricles, the resistance to be overcome being approximately the same in the two cases.


The truncus arteriosus becomes divided, much as in the chick or in the frog, by an internal longitudinal septum ; which, arising between the roots of the systemic and pulmonary arches, grows backwards in a somewhat spiral course, dividing the truncus arteriosus into right or pulmonary, and left or aortic tubes. The septum continues its growth backwards until it meets the upper free edge of the ventricular septum, with which it fuses.

After the truncus arteriosus is thus divided internally, an external groove appears on its surface, opposite the internal septum ; and this groove deepens until it splits the truncus arteriosus into two completely separate and independent vessels, of which the right one, or pulmonary trunk, arises from the right ventricle, and the left one, or aortic trunk, from the left ventricle.

The semilunar valves are formed by projections of the thickened endocardium at the roots of the pulmonary and aortic trunks : the valves are at first thick and soft, but later on become membranous.

2. The Arteries

In the rabbit, as in the chick, five pairs of aortic arches are developed, which appear in order from before backwards. By the middle of the tenth day the first two pairs are present, in the mandibular and hyoidean arches respectively. By the end of the tenth day a third pair of aortic arches is present, in the first branchial arches ; and before the end of the eleventh day the remaining two pairs are established, in the second and third branchial arches respectively.

Of these five pairs of aortic arches, the first two pairs, in the mandibular and hyoidean arches respectively, lose their connections with the dorsal aortae during the eleventh day, and become reduced to the arteries of the floor of the mouth and of the tongue.

The aortic arches of the third pair, in the first branchial arches, persist as the carotid arteries. They retain for a time their connections at their dorsal ends with the fourth pair of arches, but ultimately lose these, and from this time send blood to the head alone ; each divides into external and internal carotid arteries, supplying the parts outside and inside the skull respectively.

The aortic arches of the fourth pair, in the second branchial arches, are the systemic arches, which by their union form the dorsal aorta. At first the vessels of the two sides, right and left, are of equal size, but from a very early period the left one becomes the larger, and ultimately forms the arch of the aorta in the adult. The right systemic arch persists for some time, but ultimately disappears, with the exception of its proximal part, which is said to give origin to the right subclavian artery.

The aortic arches of the fifth pair, in the third branchial arches, are the pulmonary arches : from them the pulmonary arteries arise as posteriorly directed branches. The pulmonary arches retain their connections with the dorsal aortae throughout the whole period of intra-uterine life, up to the time of birth ; these connections having, as in the chick embryo, a most important influence on the course of the circulation. At the time of birth, the part of each pulmonary arch between the origin of the pulmonary artery and the aorta (cf. Fig. 128), a part known as the ductus arteriosus or ductus Botalli, becomes obliterated ; and from this time the blood driven into the pulmonary arches by the right ventricle can no longer pass directly to the aorta, but is all sent through the pulmonary arteries to the lungs.

Zimmermaim has found traces, in rabbit embryos of the eleventh day, of a pair of aortic arches between the systemic and pulmonary arches. This observation, if confirmed by future investigation, will be of considerable interest, as showing that the pulmonary arches of the rabbit are the sixth and not the fifth pair, and that the pulmonary arteries therefore arise in the rabbit from the same pair of arches as in the frog ; in other words, that the pulmonary arteries are strictly corresponding structures in these two types.

As regards the arteries of the trunk, the two dorsal aortae are at first distinct along their whole length, and the allantoic arteries appear as though they were direct posterior continuations of the aorta). Later on, the two aortae unite to form the definite dorsal aorta, which is continued as a narrow median caudal artery to the hinder end of the embryo ; the allantoic arteries from this time appearing as branches of the aorta.

3. The Veins

The general relations of the veins in the rabbit, and the changes which they undergo during development, are very similar to those described in the next chapter as seen in the human embryo, and will not be dealt with further in this section (cf. pp. 578 to 583).

4. The Course of the Circulation

It will be convenient to give here a brief account of the course of the circulation during the latter half of mtra-uterine life, when the placental circulation is in full swing ; and also a summary of the changes which occur at the time of birth.

As regards the heart, the ventricular septum is complete, as is also the septum of the truncus arteripsus. The auricular septum is, however, incomplete, the foramen ovale allowing blood to pass across directly from the right to the left auricle.

The blood is brought to the right auricle by the three vena? cava3. Of these, the right and left anterior venae cavae the Cuvierian veins of the earlier stages return to the heart venous blood from the head and from part of the trunk of the embryo. This is received into the right auricle and driven by it into the right ventricle.

The blood in the posterior vena cava is derived from many sources. The main factors are the allantoic veins, which return to the heart the blood from the placenta, blood which is arterial both as regards nutritive matter and as regards its contained gases.

The other factors of the posterior vena cava are, the vitelline veins from the yolk-sac, which are small and comparatively unimportant ; the mesenteric veins, which return venous blood from the alimentary canal of the embryo, and which are of small size ; and the posterior vena cava itself, which returns blood from the kidneys and the hinder part of the body. Of these factors, the allantoic veins are so much the largest that the blood returned by the posterior vena cava to the heart may be rightly spoken of as arterial. This arterial blood is discharged into the right auricle, but never really enters the cavity of the auricle, since it is directed at once, by the Eustachian valve, through the foramen ovale into the left auricle, and driven thence into the left ventricle.


The right ventricle is thus filled with venous blood, and the left ventricle with arterial blood. On the ventricular systole, the arterial blood from the left ventricle is driven through the aortic trunk and the carotid arteries to the head ; while the venous blood from the right ventricle is driven through the pulmonary trunk and pulmonary arches into the dorsal aorta, and then backwards along the body, the greater part passing along the large allantoic arteries to the placenta.

The changes that occur at birth are practically the same as those which are effected in the chick on hatching (cf. p. 314).

(i) The vitelline and allantoic circulations are stopped. The result of this is that the blood in the posterior vena cava is from this time venous, since the arterial supply previously brought by the allantoic veins is now cut off.

(ii) The ductus venosus, or direct passage through the liver, is closed. The effect of this change is that all the blood brought to the liver must now pass through its capillaries in order to get to the heart, whereas formerly the ductus venosus afforded a short cut by which the liver capillaries could be avoided.

(iii) The ductus arteriosus, or ductus Botalli, closes on both sides of the body. This renders it impossible for blood from the right ventricle to get directly into the aorta. All the blood from the right ventricle has now to pass along the pulmonary arteries to the lungs, and the pulmonary vessels consequently dilate very considerably, to accommodate this increased quantity of blood. A further effect is that the dorsal aorta now receives its blood supply from the left ventricle instead of, as formerly, from the right ventricle ; i.e. it now contains arterial, instead of venous blood.

(iv) The foramen ovale closes. This is effected at a rather later stage than the other changes. When it is completed, the blood from all three vena3 cava3 enters the right auricle, and is driven from this into the right ventricle ; while the only blood entering the left auricle is now the blood returned from the lungs by the pulmonary veins, vessels which up to the time of birth are comparatively small and insignificant, but which dilate very greatly as soon as lung breathing is established.

The circulation, by these changes, becomes that of the adult. A complete double circulation is established ; the right and left sides of the heart are perfectly distinct from each other ; and toget from one side to the other the blood must pass through either the pulmonary or the systemic circulation.

5. The Circulation in the Yolk-sac

The circulation in the yolk-sac is definitely established by the tenth day, and presents some points of interest.

In the rabbit, as in other Vertebrates, the vitelline vessels are developed in the inner, or splanchnopleuric layer of the mesoblast, beyond the embryonal area (Figs. 146 and 147). The mesoblast, as already noticed, only extends over the upper half of the blastodermic vesicle ; the lower half, or hemisphere, having a wall composed of epiblast and hypoblast alone. The boundary between these two halves is a sharp one, and is indicated by an annular vessel, the sinus terminalis (Figs. 146 and 147, Si), which runs round the margin of the mesoblast, and marks the outer limit of the vascular area.

The course of the vitelline vessels in the rabbit differs in some important respects from that of the chick. In the chick the vitelline arteries and veins lie in two layers, the veins being dorsal or superficial to the arteries ; and the sinus terminalis is a vein, which collects the blood from the marginal part of the vascular area and returns it, by branches which form main factors of the vitelline veins, to the heart (cf. Fig. 99).

In the rabbit, on the other hand, all the vessels of the vascular area lie in one plane. The vitelline arteries run straight backwards from the embryo, and open at once into the sinus terminalis, which is therefore an artery, and not, as in the chick, a vein. From the vitelline arteries themselves, and from the sinus terminalis, smaller arteries arise, which branch freely and end in capillaries ; the capillaries unite to form veins which open finally into the vitelline veins themselves, a pair of large vessels which run in the vascular area, concentrically with the sinus terminalis, but about midway between this and the embryo. Opposite the anterior or head end of the embryo, the vitelline veins turn sharply backwards, and, entering the embryo along the yolkstalk, run forwards to the heart.

There are at first two vitelline arteries, and two vitelline veins. Of the two arteries, the left one soon becomes much the larger, the right one appearing as a mere branch of it. Both vitelline veins may persist, but more usually the right one becomes much reduced in size, or else atrophies completely.

In the rabbit, the vitelline circulation is of much less importance than in the chick, inasmuch as the nutrition of the rabbit embryo is effected, not by the yolk-sac, but by the placenta.


Development of the Excretory System

The general history of the development of the excretory organs and their ducts in the rabbit is much like that of the chick.

No trace of a head kidney, or pronephros, has yet been described, and it may be assumed that this structure is either altogether absent, or else very small and rudimentary. A segmental, or Wolffian duct is early formed along each side of the body; and in connection with each duct a Wolffian body is developed, which is large in the embryo, but which becomes replaced functionally by the metanephros or permanent kidney in the later stages and in the adult animal. The Miillerian duct develops rather later than the Wolffian duct and Wolffian body ; it lies very close to the Wolffian duct, but is apparently independent of this.

1. The Wolffian Duct

The mode of development of the Wolffian duct in the rabbit has been much debated ; the point in dispute being whether it is formed from mesoblast, or directly from the external epiblast.

According to the observations of Hensen, supported by Flemming, the Wolffian duct arises, early in the ninth day, as a solid ridge-like thickening of the epiblast (Fig. 164, KG), at the level of the fourth and fifth mesoblastic somites, and close to their outer borders. It soon separates from the epiblast, and then lies as a solid rod of cells between the epiblast and mesoblast ; this rod grows rapidly backwards, becomes tubular [by the formation of an axial cavity or lumen, and on the eleventh day reaches the hinder end of the body, and opens into the dorsal surface of the allantois, just in front of the union of the rectum and the allantois to form the cloaca (e/. Fig. 150, KC, TC).

There is no doubt that the Wolffian duct, in the early stages of its development, lies very close indeed to the epiblast, especially at its hinder end ; but the more recent and very careful observations of Martin show conclusively that it is merely a case of very close apposition, and that the duct is really of mesoblastic origin along its entire length : its mode of formation being practically the same as that already described in the case of the chick, p. 315.

2. The Wolffian Body

The Wolffian body commences to form, in the latter part of the ninth or early part of the tenth day, as a series of solid strings of cells, which lie to the inner side of the Wolffian duct along almost its entire length.



FIG. 164. A transverse section across the body of a Rabbit Embryo of the early part of the tenth day, showing the supposed epiblastic origin of the Wolffian duct. (After Hensen.) x 75.

A, dorsal aorta. AN, amnion. C. coelom, or body cavity. CH, notochord. H, hyi>oblast. KG. Wolffian duct. ME, somatopleuric layer of mesoblast. MH, splanchnopleuric layer of mesoblast. MS, mesoblastic somite or protovertebra. NS, central canal of spinal cord.


These strings of cells are stated to arise as ingrowths from the peritoneal epithelium ; but the point is not definitely established, and from a very early stage the strings lie embedded in the mesoblast, and quite independent of the peritoneum. The strings soon become tubular, and are then spoken of as the Wolffian tubules. Each tubule opens at one end into the Wolffian duct ; while its opposite, or blind end, becomes expanded into a vesicle, and then doubled up on itself to form a Malpighian body, into which a branch of the aorta quickly penetrates to form the glomerulus (Fig. 165, GM). The AVolffian tubules are not segmentally arranged ; two or three corresponding to each somite in the region of the body in which they occur.

The relations of the Wolffian body to the blood-vessels are well seen in Fig. 165. The dorsal aorta, A, lies between the two Wolffian bodies, and gives off branches which supply the glorneruli ; while the posterior cardinal veins, VC, lie along their dorsal surfaces, and give off numerous branches, which lie in very close relation with the tubules, and from which the epithelial cells of the tubules withdraw the excretory products.



FIG. 1G5. A transverse section across the body of a Eabbit Embryo at the end of the eleventh day. x 45.

A, dorsal aorta. A~W, lumbar artery. C, coelom, or body cavity. CH, notochonl. GM, glomerulus of Malpighian body. GR, genital ridge. EC, Wolffian duct. KM, tubule of VVolfflim body. ME, somatopleure. MH, mesentery. NT), dorsal root of spinal nerve. NE, spinal ganglion. NN, ventral division of spinal nerve. NN', dorsal division of spinal nerve. N"S, spinal cord. WV, ventral root of spinal nerve. NY, sympathetic ganglion. TI, intestine. V, vein. VC, posterior cardinal vein.


The Wolffian body increases rapidly in size, and soon becomes more compact and of more, definite shape. Its position and relations on the twelfth tlay are well seen in Fig. 150, where the transversely running Wolffian tubules, KM, opening into the longitudinal Wolffian duct, KG, give the whole organ a somewhat comb-like appearance.

By the fourteenth day, the Wolffian body (Fig. 166, KM) has increased still further in size, especially at its hinder end ; and it remains of large size until within a short time of birth. It is the excretory organ of the embryo, and its great size and abundant vascular supply indicate that it is of considerable functional importance.




FIG. 166. A transverse section across the hinder part of the body of a Rabbit Embryo of the fourteenth day, the section passing through the hind limbs, x 12.

A, dorsal aorta. AA, allantoie artery. CH, notocliord. FC, centrum of vertebra. KG, Wolffian duct. KD, ureter, or inetanephric duct. KM, Wolffian body. KT, kidney or metanephros. LP, hind limb. ND, dorsal root of spinal nerve. NE, spinal ganglion. NN, ventral division of spinal nerve. NS, spinal cord. NV, ventral root of spinal nerve. NTT, longitudinal sympathetic cord. TA, stalk of allantois. TC, cloacal aperture on cloacal papilla. TI, intestine. VC, posterior cardinal vein.


3. The Kidney and Ureter

The adult kidney, or metanephros, develops in the rabbit in much the same manner as in the chick.


On the eleventh day a diverticulum arises from each Wolffian duct, just before this reaches the cloaca, and grows forwards dorsal to the Wolffian duct. During the twelfth day this diverticulum (Fig. 150, KD) increases in length ; its blind anterior extremity dilates, and gives rise to branching tubular processes ; while the mesoblast surrounding the processes becomes more compact than elsewhere, giving definite shape to the organ.

The structure formed in this way becomes the kidney, the original diverticulum from the Wolffian duct forming the ureter. The kidney extends forwards, dorsal to the Wolffian body, and overlapping this, so that both the Wolffian body and the kidney may be cut in the same transverse section (Fig. 166, KM and KT).

In the later stages, the lateral branches from the ureter subdivide, and elongate considerably to form the kidney tubules. There are for some time no Malpighian bodies in the kidney, but these are ultimately formed in connection with the blind ends of the tubules, in the same manner as in the Wolffian body.

The kidneys are, from the first, compact bodies ; they early acquire their characteristic shape (Fig. 160, K), and also their asymmetry in position, the right kidney moving some distance further forwards than the left.

The Wolffian duct and the ureter of each side open, on the twelfth day (Fig. 150, KG, KD), by a common duct into the urino-genital sinus. In the later stages, by unequal growth in different directions, and by absorption of the common duct into the urine-genital sinus, the relations become altered ; the Wolffian ducts still opening into the urino-genital sinus, but the ureters now opening directly into the bladder.

4. The Müllerian Duct

The mode of the development of the Müllerian duct in the rabbit has not been very clearly ascertained. About the twelfth or thirteenth day it is present as a peritoneal funnel, lying to the inner side of the Wolffian body, close to its anterior end ; from the funnel a duct arises which crosses over, dorsal to the Wolffian body, and then runs backwards a short distance, lying very close to the outer side of the Wolffian duct, and ending blindly behind. During the succeeding days the Müllerian duct grows slowly backwards, but does not reach the level of the Brine-genital sinus until about the twentieth day.

5. The Genital Ducts and Accessory Genital Organs

In the male, or buck rabbit, outgrowths from the tubules of the Wolffian body penetrate into the testis at a very early stage of development, forming the tubuliferous tissue already described, and giving rise ultimately to the vasa efferentia. The Wolffian body becomes greatly reduced in size, and is converted into the head of the epididymis ; the proximal part of the Wolffian duct, which is greatly convoluted, gives rise to the body and tail of the epididymis (Fig. 160, w) ; and the distal part of the duct forms the vas deferens, x.

The testes originally lie opposite the anterior ends of the Wolffian bodies, and attached to the dorsal wall of the abdomen ; ultimately they shift their position from the dorsal to the ventral wall of the abdomen, and, passing through the inguinal rings, become lodged in a pair of pouch-like folds of the skin, the scrotal sacs (Fig. 160).

The Miillerian ducts, in the male rabbit, disappear completely. The uterus masculinus (Fig. 160, s)has been stated to be formed from their hinder or distal ends, but according to Kolliker it is derived from the Wolffian, and not from the Miillerian ducts ; these latter in the male never opening into, or even reaching, the urino-genital passage.

In the female, or doe rabbit, the Miillerian ducts become greatly enlarged, and form the oviducts. Their abdominal openings persist as the open fimbriated mouths of the Fallopian tubes ; the proximal portions of the ducts become the Fallopian tubes themselves ; the middle portions become the uteri ; and the terminal, or distal segments unite to form the vagina.

The Wolffian bodies, in the female, undergo degenerative changes ; they become greatly reduced in size, and are ultimately converted into the parovaria. The Wolffian ducts either disappear completely, or else small portions of them persist as rudimentary or vestigial structures.

Development of the Coelom

The coelom, or body-cavity, of the rabbit appears, as in most Vertebrates, as a cleft in the mesoblast, formed by splitting, or rather by rearrangement, of its cells into two layers, somatic and splanchnic.

The coeloun appears first on the eighth day, and by the ninth day (Fig. 1 16, c) has become a cavity of considerable size. It is not confined to the embryo, but stretches out beyond this, and in all directions, reaching almost to the margin of the mesoblast, indicated by the sinus terminalis, Si.

Immediately in front of the embryo, in the pro-amnion (Fig. 145, AN 1 ), there is at first no mesoblast, and consequently no coelom ; but in the later stages, as the mesoblast invades the proamnion from its sides, the coelomic cavity extends into this region also.

Within the embryo itself, the coelom is confined to the body region, and does not extend forwards into the head. The abdominal portion of the coelom presents no further changes of special interest, but in the thorax the development of the pericardial and pleural cavities, and also the formation of the diaphragm, require notice.

1. The Pericardial Cavity

Early on the ninth day, the heart consists of two tubes, lying along the sides of the head, and widely separate from each other (Fig. 145, R). The parts of the ccelom into which these tubes project become later on the pericardial cavity, so that this cavity, like the heart itself, consists at first of two separate halves, right and left respectively.

As the side-folds deepen, the two halves of the heart are brought together beneath the pharynx ; and, early on the tenth day, the right and left halves of the pericardial cavity meet beneath the throat, and become continuous with each other.

The pericardial cavity (Fig. 147) is thus merely the anterior part of the general body-cavity or coelom, and there is at first no boundary between the two, except the very imperfect partitions formed by the right and left vitelline veins, where they diverge behind the heart.

Towards the close of the tenth day, and during the early part of the eleventh day, the pericardial cavity becomes shut off from the body cavity by a couple of septa. One of these, which is ventral in position, is formed by a thick transverse fold of the splanchnopleuric mesoblast, immediately behind the heart, and between this and the liver. The second, or dorsal septum is much thinner, and grows forwards from the walls of the Cuvierian veins to the anterior end of the body cavity. These two septa, between them, shut off the ventral and anterior portion of the coelom as a pericardial cavity, distinct from the general body cavity (Figs. 150 and 103, CP).

2. The Pleural Cavities

After the boxing-in of the pericardial cavity, by the dorsal and ventral septa, is completed, the general body cavity still extends forwards as a pair of pocket-like diverticula, dorsal to the pericardial cavity, and along the sides of the oesophagus. Into these pocket-like cavities the lungs hang freely, and the pockets themselves become the pleural cavities.

As the lungs enlarge, the pleural cavities, which at first lie entirely dorsal to the pericardial cavity, gradually extend downwards so as to embrace its sides (Fig. 163, CK), and ultimately reaching almost to the mid-ventral wall of the chest.

3. The Diaphragm

The diaphragm is formed from a couple of septa, dorsal and ventral respectively, which arise independently, and are for some time quite distinct from each other.

Of these, the ventral septum is the thick transverse partition already described as forming the ventral part of the hinder wall of the pericardial cavity.

The dorsal septum of the diaphragm arises, on the thirteenth day, as a transverse fold of mesoblast, which grows downwards from the dorsal wall of the body cavity, just behind the Cuvierian veins. It has for a time a free ventral edge, crescentic in shape; but it ultimately meets, and fuses with, the ventral septum, or posterior wall of the pericardial cavity, thereby completing the diaphragm, and shutting off the pleural cavities from communication with the body cavity.


Development of the Muscular System

The majority of the body muscles are developed, as in the chick, from the muscle plates of the protovertebra3, or mesoblastic somites.

The great dorsal muscles of the neck and trunk, and the muscles of the thoracic and abdominal walls, are derived directly from the muscle plates, but the origin of many of the other muscles is not determined with certainty. The muscles of the head arise independently of the muscle plates ; and the muscles of the limbs also arise independently, and in situ. It is probable, however, that in both these cases the mode of development has undergone secondary modifications and abbreviations.


Development of the Skeleton

There are in the rabbit, as in the chick or frog, three stages in the development of the skeleton. The first, or earliest, stage is that in which the notochord is the only specially skeletal structure present; the second stage is that in which a cartilaginous skeleton is developed, not only in relation with the notochord, but in the head and limbs as well ; while the third or final stage is characterised by the development of bone, which gradually becomes the dominant and essential constituent of the skeleton. Bones arise either as cartilage-bones, in direct connection with the cartilaginous skeleton ; or else independently of this, as membrane-bones.

It is important to remember that each of these stages is not a further development of the preceding stage, but an independently arising one, which displaces its predecessor. Thus the cartilaginous skeleton does not arise from the notochord, but outside this and independently of it, and gradually displaces and obliterates it; to be displaced in its turn by the bony skeleton. So too the lower jaw is not formed from Meckel's cartilage, but around it ; and the formation of the bone leads ultimately to the obliteration of its cartilaginous predecessor.

The development of the skeleton of the rabbit has not yet been studied in detail, and there are many points on which our knowledge is still very incomplete.


1. The Vertebral Column

On the tenth day, the notochord, which up to this time has been the sole skeletal structure present, becomes surrounded by a membranous sheath ; and, during the eleventh and twelfth days, a cartilaginous tube begins to form around this sheath.

By the fourteenth day, the cartilaginous tube is definitely established ; and in it a distinction, as regards histological characters, is apparent, from the first, between the vertebral and the intervertebral regions. The tube thickens on its inner surface, and so begins to encroach upon the notochord. Opposite the centra of the vertebras the notochord becomes constricted, and finally completely obliterated.

Between the successive vertebrae, in the intervertebral regions, the notochord remains of full width for a long time ; and, according to Kolliker and others, it even persists throughout life, as part of the nucleus pulposus in the axes of the intervertebral ligaments.

From the vertebral centra the neural arches (Fig. 163, FN) grow up at the sides of the spinal cord, during the fifteenth and sixteenth days ; but the completion of the neural canal dorsally does not occur until a late stage.

The first two vertebras undergo modifications similar to those already described in the bird ; the centrum of the first vertebra or atlas (Fig. 167) separating from the rest of the vertebra, and fusing with the centrum of the second, or axis, vertebra to form its odontoid process.

The transverse and other processes of the vertebras arise as outgrowths from the cartilaginous centra or from the neural arches.

2. The Ribs and Sternum

The ribs (Fig. 163, RI) arise as bars of cartilage, in the connective tissue septa between the several muscle-segments or myotomes of the thorax. In the rabbit, the two or three most anterior ribs are at first continuous with the vertebras, and appear as elongated transverse processes. At a later stage a joint is formed between the rib and the vertebra, and in this way the tubercular articulation is acquired (cf. Figs. 163 and 167). The head or capitulum of the rib develops as an outgrowth from the proximal end of the rib, and does not articulate with the vertebra until a considerably later period. The posterior ribs, behind the first two or three, develop from the start independently of the vertebrae.



FIG. 167. Selected vertebrae from the Eabbit. (From Marshall and Hurst.)

I. First cervical vertebra, or atlas, from the dorsal surface. II. Second cervical vertebra, or axis, from the right side. III. Fifth cervical vertebra ; anterior surface. IV. Fourth thoracic vertebra, from the right side.

V. Fourth thoracic vertebra, and fourth pair of ribs ; anterior surface.

VI. Second lumbar vertebra, from the right side. VII. Second lumbar vertebra ; anterior surface.

AP, anapo]>hy*is. AZ, anterior, or pre-zygapophysis. C, centrum. CE. epiphysis of centrum. GEL, cervical rib. FH, facet for capitulum or head of the fourth rib. FH', facet for capitulum of the fifth rib. FO, facet for odontoid process. FT, facet for tubercle of fourth rib. HP, hypapophysis. MP, nietapophysis. NS, neural spine, or spinous process. OP, odontoid process. PZ, ]>ost-zygapophysis. RC, capitulum or head of rib. RP, process of rib for attachment of ligaments. RS, sternal portion of rib. RT, tubercle of rib. RV, vertebral portion of rib. S, sternum. TP, transverse process. VA, vertebrarterial canal. Z, articular surface for axis vertebra.



The sternum is formed in two halves, and from the ventral ends of the ribs. Each rib is at first slightly dilated at its ventral end (Fig. 163, ST), and these enlarged ends of successive ribs, growing both anteriorly and posteriorly, meet and fuse, so as to form along either side a longitudinal cartilaginous bar, connecting the ventral ends of the ribs of its side of the body. The two bars, right and left, approach each other, meet in the median plane, and fuse to form the sternum.

3. The Skull

(cf. Figs. 160 and 162).

The cartilaginous skull of the rabbit is formed from the same essential elements parachordals, trabeculas, sense capsules, and visceral bars as in the chick or frog ; and the general relations of these parts to one another are very similar in the three animal?. Cartilage appears in the head of the rabbit embryo about the fourteenth day, and by the sixteenth or seventeenth day the cartilaginous skull is practically completed.

The two parachordal cartilages fuse together very early to form the basilar plate (Fig. 151, RP), which underlies the medulla oblongata, and forms the floor of the hinder part of the skull. The edges of the basilar plate grow up at the sides of the brain, and fuse with the independently arising periotic capsules (Fig. 159, EC) ; and then, growing in towards each other, meet above the cerebellum to complete the occipital ring (Fig. 151, ox). In front of the supra-occipital cartilage, the roof of the skull remains membranous until the formation of the bones.

The trabeculae are a pair of rods of cartilage, which are continuous at their hinder ends with the basilar plate : further forwards they lie at the sides of the pituitary body, and in front of this unite to form the ethmoidal plate (Fig. 151, ET). This latter is at first small, and never becomes so large as in the bird, but as the nose grows forwards, and the face assumes its definite form, the ethmoidal plate extends forwards with it, giving off from its upper surface a median vertical septum between the two olfactory organs. The cartilaginous olfactory capsules arise independently, but very early fuse with the ethmoidal septum.


With regard to the cartilaginous bars developed in the visceral arches, the maxillary or palatopterygoid bar forms the basis of the upper jaw, but it is not clear whether it arises independently, or as an outgrowth from the mandibular bar.

The mandibular bar is a rod of cartilage, which along the greater part of its length is known as Meckel's cartilage (Figs. 151 and 156, MC) ; it forms the basis of the lower jaw, the bones of the mandible being formed around it, though not in direct connection with it, except at the chin.

The hyoid bar is at first cartilaginous along its whole length, but subsequently disappears in great part. Its lower or ventral end forms the basis of the anterior, or lesser cornu of the hyoid bone of the adult.

Of the first branchial bar, the only part that persists is the ventral end, which forms the basis of the posterior, or greater cornu of the hyoid bone. The body of the hyoid bone is formed from the median elements of the hyoid and first branchial arches.

The development of the auditory ossicles, and their relations to the mandibular and hyoid bars have already been considered in the section dealing with the development of the ear (p. 398).

Concerning the appendicular skeleton there is nothing special to note, except that Kolliker has shown that the clavicle in rabbit embryos of about the seventeenth day is cartilaginous ; and that the clavicle, though presenting some peculiarities in the details of its mode of ossification, ought to be viewed as a cartilage bone, and not, as is commonly stated, as a membrane bone.

Development of the Skin

1. The Hairs

Hairs are epidermal structures, and are as characteristic of Mammals as are feathers of Birds. The first stage in the formation of a hair consists in the growth of a small solid process from the deeper or mucous layer of the epidermis, into the underlying connective tissue (Fig. 15G, DE). A small papilla of vascular connective tissue grows into the deeper end of the epidermal process, and serves for its nutrition. The hair itself is formed by cornification of the axial or central cells of the pi'ocess, while the outer or peripheral cells form the hair-sheath, or follicle. The hair grows upwards from its base, and the free tip soon projects above the surface of the skin.

From the first, the hairs of the eyebrows, and of the upper lip and nose are of exceptionally large size (Fig. 149) ; and one particularly large hair, arising from the cheek immediately below the eye, forms a prominent feature in rabbit embryos from about the nineteenth day onwards, and is also very large in the adult rabbit.

2. The Claws

The claws are formed by cornification of the epidermis at the ends of the fingers and toes. The layer of epidermis that becomes converted into the claw is not, in the first instance, the most superficial one, but is a special stratum, developed between the superficial and the deeper or Malpighian layers of the epidermis ; the Malpighian layer, with the underlying dermis, being modified to form the bed of the claw. The distal border of the claw soon projects freely at the end of the digit, and its further growth is effected by additions at its hinder or attached border, and to its under surface.

3. The Mammary Glands

The mammary glands, like the other cutaneous glands, are formed by ingrowths of the epidermis into the underlying connective tissue. These ingrowths give off secondary branches, which are at first solid, but soon become hollow, and form the gland cavities ; the ducts being derived from the original epidermal ingrowths.

Development of the Placenta

The placenta is the organ by which the nutrition of the embryo is effected during the period of its stay in the uterus ; and it is through the placenta that the mammalian embryo is enabled to attain so large a size, and so high a grade of development at the time of birth, although formed from an ovum of extremely small size and almost devoid of food-yolk.

The placenta (Fig. 170) is formed partly from the mother, and partly from the embryo or foetus ; the foetal element being supplied by the wall of the blastodermic vesicle, and by the allantois ; and the maternal element by the part of the wall of the uterus to which the blastodermic vesicle becomes attached.

In the chick, the allantois (Fig. 101) attains a great size, and forms the respiratory organ of the embryo during the later stages of its development.

In the rabbit the allantois becomes still larger and more important, subserving nutrition as well as respiration. It becomes firmly attached to the wall of the uterus (Figs. 148 and 170), and then gives off, from its outer surface, vascular tufts or villi into the substance of the uterine wall. The vessels of these villi, which are derived from the allantoic arteries and veins, and are therefore continuous with the blood-vessels of the embryo, lie in close contact with the dilated maternal capillaries of the uterus. The intervening walls between the two sets of bloodvessels, foetal or allantoic, and maternal or uterine, become so greatly reduced in thickness that diffusion readily takes place between the two blood streams, through these very thin partitions. In this way the fcetal blood derives nutrient matter from the maternal blood, and gives up to it the gaseous and other excretory matters that are formed in the embryo, as a necessary consequence of the chemical changes associated with its growth and development.

The actual details of development of the rabbit's placenta are extremely complicated, and the accounts given by different investigators are at variance with one another, even in points of primary importance. The most complete and consistent account is that given by Duval ; it is supported in many important respects by Miuot's investigations, and has afforded the basis on which the following description has been founded.

The mucous membrane of the uterus, in the unimpregnated condition, is thrown into six longitudinal folds, which project into the uterine cavity, and give it a stellate appearance in transverse section. Of these folds, two (Fig. 168, PK) lie on the side of the uterus next to the mesometrium, or mesenterial fold, MM, which attaches the uterus to the abdominal wall ; these are termed by Minot the placental folds or placental lobes. The second pair, or periplacental folds, P.M. lie at the sides of the uterus ; and the third pair, or obplacental folds, lie opposite the placental folds, along the free or unattached border of the uterus.

It is from the mesometrial, or placental, folds alone that thematernal part of the placenta is derived : the periplacental and obplacental folds undergo considerable changes, but do not take any direct part in the formation of the placenta.


FIG. 168. A transverse section across the uterus, with the contained blastodermic vesicle, of a Rabbit at the end of the seventh day. (In part after Duval.) x 12.

E, epiblast of blastodermic vesicle. EK, thickened epiblast of embryonal area. GTJ, uterine glands. H, hypoblast of blastodermic vesicle. MI, outer or longitudinal muscles of the wall of the uterus. MK, inner or circular muscles of the wall of the uterus. MM, mesometrium, or mesenterial fold connecting the uterus with the dorsal wall of the abdomen. PK, placental fold of uterus. PM, peri placenta! fold of uterus. PR, median cleft between the two placental folds. UC, dilated capillaries of submucous layer of uterus. YS, yolk-sac.


On the seventh day the blastodermic vesicles are spaced out along the uterus, and the swellings or loculi of the uterus, indicating their position, are well marked externally.

The blastodermic vesicle, the structure of which at this stage has already beeii described (p. 360), lies quite freely within the uterus, and the structure of the uterine walls is as follows (cf. Fig. 168).

The muscular walls of the uterus are well marked, consisting of outer longitudinal, MI, and inner circular layers, MK. Within the layer of circular muscles come the submucous and glandular layers. Of the six longitudinal folds of the uterus, the two placental folds, PK, form large and prominent ridges, separated by a deep median cleft, PR. The periplacental folds, PM, are similar, but much smaller ; while the obplacental folds are no longer recognisable, having become flattened out and obliterated by the stretching, which this part of the wall of the uterus has undergone, to make room for the embryo.

The submucous layer, which is very thick in the placental folds, PK, but comparatively scanty elsewhere, consists of loose connective tissue, with very numerous, branched connectivetissue cells, and is very vascular. The blood-vessels, which are derived from the mesometrium, perforate the muscular walls of the uterus as small arteries and veins, and then dilate, within the submucous layer, into large but very thin-walled capillaries (Fig. 168, UC), which are especially numerous in the subglandular layer of connective tissue, immediately below the surface epithelium.

The epithelium lining the uterus is pitted to form the uterine glands, GU, which are very deep and freely branched in the placental and periplacental folds ; while in the obplacental area, owing to the stretching which this part of the uterus has undergone, the mouths of the glands are greatly dilated, and the glands themselves widened out.

Early on the eighth day the attachment of the blastodermic vesicle to the wall of the uterus commences, and by the ninth day it is completed. The attachment is effected, as already noticed, by thickening and proliferation of the epiblast cells of the blastodermic vesicle over a horse-shoe shaped patch, the placental area, which surrounds the sides and hinder end of the embryo (Fig. 145, E'). The epiblast cells of this placental area become more numerous, by repeated divisions, and grow out into irregular processes which fuse firmly with the surface of the placental lobes of the uterus (Fig. 169, E). By this time, according to Duval, the uterine epithelium of the placental lobes has entirely disappeared, by absorption, though it remains unaltered in the deeper parts of the glands for some time longer : the embryonic epiblast of the placental area is, therefore, in direct contact with the connective tissue of the uterine wall.

This thickened epithelium of the placental area of the blastodermic vesicle is a structure of very great importance, and has been named by Duval the ectoplacenta. It serves in the first instance, as just noticed, to attach the embryo to the uterine wall, and in the later stages it plays a very prominent part in the formation of the placenta. It must be borne in mind throughout the following description that, if Duval's account is correct, the ectoplacenta is entirely of foetal origin, and is not derived, even in part, from the uterine epithelium. This is a point, however, 011 which difference of opinion obtains ; Strahl, for instance, maintaining that the ectoplacenta is formed by proliferation of the uterine epithelium, and not from the embryonic epiblast.

The embryo normally lies with its long axis coinciding with that of the blastodermic vesicle, and therefore with that of the uterus, so that a transverse section of the uterus cuts the embryo transversely (Fig. 169, XG). The embryo is usually in the middle of the upper surface of the blastodermic vesicle, and lies opposite the deep cleft, TR, between the two placental lobes, The position of the embryo is, however, variable, especially in the earlier stages : it may lie obliquely across the vesicle ; or may, more rarely, lie opposite one or other of the placental lobes, instead of opposite the cleft between them.

In the submucous layer of the placental lobes important changes occur during the ninth day. The capillaries dilate very considerably (Fig. 169, uc), becoming much larger than the arteries and veins in connection with them. They retain their simple epithelial walls, but thick adventitious perivascular walls are formed outside these by the surrounding connective-tissue cells. These perivascular cells are at first ordinary connectivetissue cells, which increase in number, draw in their processes,, and become arranged in layers, two or three cells thick, around the capillaries. This perivascular thickening of the walls of the capillaries occurs throughout the greater part of the submucous. layer, but does not affect the capillaries immediately beneath the surface of the uterus, nor those of the outermost layer, next to the circular muscles of the uterine wall.


FIG. 169. A transverse section across the uterus and the contained blastodermic vesicle of a Rabbit at the end of the ninth day. Cf. Figs. 145 and 146, in which the blastodermic vesicle and embryo of this age are shown in surface view and in sagittal section. (In part after Duval.) x 8.

AN, side fold of the amnion. C, mesoblast of the upper wall of the blastodermic vesicle, beyond the embryonal area. E, epiblast of the blastodermic vesicle ; the upper reference is to the thickened epiblast of the placental area. GTJ, uterine glands. G"W, modified uterine glands of placental region. H, hypoblast of blastodermic vesicle. MI, outer or longitudinal musoles of the wall of the uterus. M K, inner or circular muscles of the wall of the uterus. MM, mesometriuin. N G, neural groove of embryo, in transverse section. PR, median cleft between the placental lobes of the uterus. SI, sinus terminalis. UC, capillaries of placental region, with thickened perivascular walls. ITL, giant cells. T7V, blood-vessels of uterus. YS, yolk-sac, or cavity of blastodermic vesicle.

During the tenth day, the ectoplacental epithelium increases greatly in thickness, and becomes excavated by irregular channels or lacunae, which according to Duval open into the maternal or uterine capillaries. At the same time the inner or deeper surface of the ectoplacenta is becoming folded, and the mesoblast of the somatopleure grows in between these folds (cf. Fig. 147, E'). The uterine glands of the placental lobes have by this time almost disappeared (cf. Fig. 169,G\v); and' a little later they are completely absorbed. In the submucous layer the peri vascular thickening of the walls of the capillaries has proceeded still further, while the capillaries themselves are even larger than before ; and ultimately nearly the whole of the connective tissue of the submucous layer becomes converted into perivascular, or, as they are now termed, decidual cells.

In the periplacental lobes somewhat similar changes occur. The superficial epithelium of the uterus, and the epithelium lining the mouths of the glands degenerate and disappear ; and perivascular thickenings of the capillary walls occur, although to a less marked extent than in the placental lobes.

In the obplacental region also, the uterine epithelium degenerates and becomes absorbed ; but the epithelium of the glands themselves remains, and at a later stage, by spreading outwards from the mouths of the glands, reconstitutes an epithelial lining to this part of the uterus.

Towards the end of the tenth day, and during the eleventh day, the allantois is growing rapidly. As shown in Figs. 146 and 147, the outer or rnesoblastic wall of the allantois very early coalesces with the mesoblast of the outer layer of the amnion, opposite the placental area ; and in this way the blood-vessels of the allantois are brought immediately beneath the ectoplacental epithelium, and consequently into close proximity with the dilated capillaries of the uterus : and the placenta is thus established.

The further development of the placenta consists mainly in a gradually increasing complication and elaboration, by which folds of the mesoblast, containing the allantoic vessels, are carried deeply into the ectoplacenta from its inner surface ; while from the outer surface the maternal vessels extend in further, and in larger numbers, than before. This interdigitation of the foetal and maternal blood-vessels is accompanied by progressive thinning of the layer of ectoplacental epithelium intervening between them, until ultimately the two sets of Wood-vessels are separated by exceedingly thin partitions.

The successive steps in this process are as follows ; Duval's descriptions being mainly followed in the account here given.

From the tenth day onwards the growth of the vascular septa, or villi, from the allantois into the ectoplaceiita proceeds very rapidly, so that the latter becomes cut up into a series of radially ai-ranged columns, or lobules, within which lie the lacunas opening into the maternal capillaries. At this stage the fcetal blood is separated from the maternal blood by three structures : (i) the endothelial wall of the fcetal or allantoic capillaries ; (ii) a layer, several cells in thickness, of the ectoplacental epithelium ; (iii) the endothelial wall of the maternal -capillaries. There is some doubt, however, with regard to the third layer ; according to Duval, this has already disappeared, and the maternal vessels of the placenta are merely lacunar spaces hollowed out in the ectoplacental epithelium, and devoid of true walls.

During the twelfth to the fourteenth days, each of the ectoplacental columns or lobules becomes subdivided, by longitudinal folding of its walls, and ingrowth of septa, into a set of closely placed parallel tubules, the general direction of which is radial, i.e. vertical to the inner surface of the uterus.

These lobules, in the later stages, become larger and more minutely subdivided, and by the nineteenth or twentieth day the relations are as shown in Fig. 170. Each of the two placental lobes now consists of a number of lobules, rn, which are somewhat fusiform in shape, radially arranged, and packed closely together side by side. Each lobule is further subdivided into a complicated system of branching tubular passages, which at ^ach end of the lobule open into larger chambers, UP. Through these passages, which, according to Duval, are simply lacunae excavated in the ectoplacental epithelium, the maternal blood circulates. Large afferent channels, derived from the uterine arteries, convey the maternal blood directly to the dilated chambers at the inner ends of the lobules, next to the surface of the uterus. From these chambers it flows back, through the complicated system of tubules of which the lobule consists, to the chambers at the outer ends of the lobules, from which it is carried away by efferent vessels which open into the uterineveins.

The foutal or allantoic vessels, AA, pass between the several lobules to their outer ends, and then return as thin-walled capillaries, which pass through the lobules, lying between the tubules into which these are divided ; on reaching the inner surface of the uterus the capillaries open into the allantoic veins,. VA, which return the blood from the placenta to the embryo.

In the later stages, from the twenty-fifth to the thirtieth day, the chief changes consist in the gradual thinning of the partitions separating the foetal and maternal streams in the lobules. The ectoplacental wall becomes gradually absorbed, more and more completely, until ultimately, according to Duval, a single layer of epithelial cells, the endothelial wall of the foetal capillary, is alone left between the two streams of blood.

The changes that occur in the deeper, or submucous part of the placenta require further notice. In the early stages (Fig. 169), the submucous layer is very thick, and the ectoplacenta very thin. By the nineteenth day (Fig. 170) the two have become of about equal thickness. From this time the submucous layer is the thinner of the two, and towards the close of gestation it becomes comparatively insignificant.

The chief changes that occur in the submucous layer during these later stages are : a still further dilatation of the capillary vessels ; an increase in the decidual cells surrounding the capillaries ; and the appearance in the subglandular region, of a layer of special cells, spoken of as glycogenous cells. These latter are large, roundish, or ovoid vesicular bodies, each consisting of an outer capsule and a central multinucleate protoplasmic body, from which strands of protoplasm radiate outwards to the capsule. In the meshes between the strands lie faintly glistening glycogen masses. Each of these glycogenous cells is said to beformed by the fusion of a number, from three to six, of originally separate cells.

The perivascular and glycogenous cells are probably to be regarded as having some function in connection with the elaboration, or preparation, of the maternal blood, before it is sent to the placenta for the nourishment of the embryo. The blood in the maternal capillaries of the placenta is specially characterised by the relatively enormous number of leucocytes which it contains, at all stages from about the eleventh or twelfth day onwards.



FIG. 170. A transverse section across the uterus and the contained embryo of a Rabbit at the end of the nineteenth day. The embryo is cut transversely, about the middle of the body, the section passing through the yolk-stalk and allantoic stalk, x 3|.

A, dorsal aorta of the embryo. AA, allantoic arterv. AX, amnionic cavity, between the inner or true ainniou iiml the embryo. CX, s]>ace between the inner and outer layers of the amnion ((/. Fig. 148). Q-U, uterine glands of obplacental region. TT, iiypoblast of upper or vascular wall of yolk-sac. MI, outer or longitudinal muscles of the wall of the uterus. MK. inner or" circular muscles of the wall of the uterus. MM, mesometrium. NS, spinal cord of the embryo. NY, sympathetic nerve cord. PH, lobule of placenta. PO. region along which the separation of the placenta occurs at birth. PR, interplacental grtnive. P W, subplacental cavity. SI, sinus terminalis. TA, cavity of the allantois <</. Fig. 148). TS, stomach of embryo. UC, dilated uterine capillary, with thick peri vascular wall. UP, uterine or maternal sinuses of placenta. U V, blood-vessels of uterus. VA, allantoic vein. W, liver of embryo. YK. yolk-stalk. YL. dotted line representing the lower or non-vascular wall of the yolksac, now completely absorbed. YS, cavity of yolk-sac, continuous with the uterine cavity owing to absorption of the lower wall of the yolk-sac.


Curious modifications occur in the lining epithelium of the maternal capillaries of the submucous layer during the formation of the placenta. The ordinary endothelial walls, which these vessels at first have, become replaced by a layer of irregular, thickened, and often columnar cells. According to Duval, this layer is formed by extension outwards of cells from the ectoplacenta along the interior of the maternal vessels ; while Minot regards it as formed by degenerative changes in the proper endothelial wall of the capillaries.

In the obplacental region, and to a less extent in the periplacental region, certain peculiar cells, characterised chiefly by their enormous size, and hence spoken of as colossal or giant cells, appear in the submucous layer at an early stage (Fig. 169, UL). These are stated to be derived from the uterine epithelium of these regions ; they form marked features from the ninth day onwards, but their function is entirely unknown. Cells of exceptional size are commonly associated with absorptive, rather than with formative changes, but the actual absorption occurring in this region of the uterus is comparatively slight in amount.

Parturition. The outer layer of the submucous connective tissue, next to the circular muscle layer of the uterus, is characterised by the small size of its blood-vessels (Fig. 170, PO) ; and it is along this line that separation takes place at the time of birth, the entire placenta, both foetal and maternal, coming away with the young animal.

The actual separation is effected by strong contractions of the muscles of the uterus. The haemorrhage at parturition is but slight, partly because the blood-vessels along the plane of separation are small, and partly because of the rapidity with which complete contraction of the uterus is effected.

Long before the birth of the young animal, the mucous membrane of the obplacental region of the uterus has been completely re-established ; this mucous membrane is attached to the muscular walls of the uterus by very loose connective tissue. Owing to the strong contraction of the muscles of the uterus at the time of birth of the young, the bare patch, from which the placenta has been separated, is at once greatly reduced in size, while the loosely attached mucous membrane of the obplacental region slips over it, and closes the wound almost instantly. The complete regeneration of the uterine epithelium after parturition is effected with astonishing rapidity, and the doe is ready to receive the buck almost immediately after she has given birth to the young.

The placenta is commonly regarded as essentially an allantoic structure. But the facts, that the attachment to the uterus is first effected, not by the allantois, but by the epiblast of the blastodermic vesicle ; and that the allantois merely utilises this attachment as a means of getting access to the uterus, suggest that the participation of the allantois in the formation of the placenta is probably a secondary and not a primitive character.

The further fact that changes occur in the mucous membrane of the obplacental and periplacental regions, similar to the earlier changes seen in the placental region, suggests that the area of attachment of the blastodermic vesicle to the uterus was originally a more extensive one. Minot has contended, from these and similar considerations, that the mammalian placenta was originally formed from the chorioii, i.e. from the extra- embryonic part of the blastodermic vesicle, and not from the allantois ; and the history of the formation of the placenta in the lower groups of Mammals strongly supports this view.

Bibliography

List of the more important Publications dealing with the Development of the Rabbit.


Barry. M. : ' Researches in Embryology.' Philosophical Transactions of the Royal Society. 1840.

Beneden, E, van: ' Recherches sur la Composition et la Signification deTCEuf.' Bruxelles. 1870.

'Recherches sur 1'Embryologie des Mammiferes. La Formation des Feuillets chez le Lapin.' Archives de Biologie, i. 1880.

' Observations sur la Maturation, la Fecondation et la Segmentation de 1'CEuf des Cheiropteres.' Archives de Biologie, i. 1880.

Beneden, E. van, and Julin, C. : Recherches sur la Formation des Annexes Fcetales chez les Mammiferes.' Archives de Biologie, v. 1884.

BischofT, T. L. W. : ' Entwicklungsgeschichte des Kaninchen-Eies.' Braun-. schweig. 1842.

Born, G. : ' Beitrage zur Entwickelungsgeschichtc des Saugethierherzens. Archiv fur mikroskopische Anatomic, xxxiii. 1 889.

Coste, M. : ' Histoire generale et particuliere du Developpement des Corps organises.' Paris. 1847-1859.

Duval, M. : ' Le Placenta des Rongeurs.' Journal de 1'Anatomie et de la Physiologic, xxv. and xxvi. 1889-9(1.

Flemming, W. : ' Ueber die Bildung von Richtungstiguren in Siiugethiereiern beim Untergang Graaf'scher Follikel.' Archiv fiir Anatomie und Ent wickelungsgeschichte. 1885.

'Die ektoblastische Anlage des Urogenitalsystems beim Kanin chen.' Archiv fiir Anatomie und Entwickelungsgeschichte. 1886.

Foster, M.,and Balfour, F. M. : 'The Elements of Embryology;' second edition by Sedgwick and Heape. 1883.

Fraser, A. : 'On the Development of the Ossicula Auditus in the Higher Mammalia.' Philosophical Transactions of the Royal Society. 1882.

Goette, A. : ' Beitrage zur vergleichenden Morphologic des Skeletssystems der Wirbelthiere.' Archiv fur mikroskopische Anatomie, xiv. 1877.

Haddon, A. C. : ' Suggestions respecting the Epiblastic Origin of the Segmental Duct.' Scientific Proceedings of the Royal Dublin Society. 1887.

Hensen, V. : ' Beobachtungen iiber die Befruchtung und Entwicklung des Kaninchens und Meerschweinchens.' Archiv fiir Anatomie und Knt wickelungsgeschichte. 1875.

Hochstetter, F. : ' Ueber die urspriingliche Hauptschlagader der hinteren Gliedmasse des Menschen und der Siiugethiere.' Morphologisches Jahrbuch, xvi. 1890.

Hubrecht, A. A. W. : ' Studies in Mammalian Embryology : i. The Placenta tion of Erinaceus Europams. with Remarks on the Phylogeny of the Placenta.' Quarterly Journal of Microscopical Science, xxx. 1889.

Huxley, T. H. : 'Evolution and the Arrangement of the Vertebrata.' Proceedings of the Zoological Society. 1880.

Kastschenko, N. : ' Das Schicksal der embryonalen Schlundspalten bei Sauge thieren.' Arcliiv fiir mikroskopische Anatomie, xxx. 1887.

Kolliker, A. : ' Entwicklungsgeschichte des Menschen und .der hoheren Thiere.' Leipzig. 1879.

' Ueber die Chordahohle und die Bildung der Chorda beim Kaninchen.'

Sitzungsberichte der phys.-med. Gesellschaft in Wiirzburg. 1883.

' Die Entwicklung der Keimbliitter des Kaninchens.' Leipzig. 1882.

Krause, W. : ' Die Anatomie des Kaninchens.' Leipzig. 1868.

Lockwood, C. B. : ' The Early Development of the Pericardium, Diaphragm, and Great Veins.' Philosophical Transactions of the Royal Society. 1888.

Lowe, L. : ' Beitrage zur Anatomie und zur Entwickelungsgeschichte des Nervensystems der Siiugethiere und des Menschen.' Berlin. 1880.

Martin, E. : ' Ueber die Anlage der Urniere beim Kaninchen.' Archiv fur Anatomie und Entwickelungsgeschichte. 1888.

Masius, J. : ' De la Genese du Placenta chez le Lapin.' Archives de Biologic, ix. 1889.

Masquelin, H., and Swaen, A.: 'Premieres phases du Developpement du Placenta maternel chez le Lapin.' Archives de Biologie, i. 1880.


Minot, C. S. : Uterus and Embryo. I. Rabbit. II. Man.' Journal of Morphology, ii. 1889.

' Die Placenta des Kaninchens.' Biologisches Centralblatt, x. 1890. ' Zur Morphologie der Blutkorperchen.' Anatomischer Anzeiger, v. 1890.

' A Theory of the Structure of the Placenta.' Anatomischer Anzeiger, vi. 1891.

Owen, R. : ' Comparative Anatomy and Physiology of Vertebrates,' iii. 1868.

Parker, W. K. : ' Mammalian Descent.' London. 1885.

Paterson, A. M. : ' Development of the Sympathetic Nervous System in Mammals.' Philosophical Transactions of the Royal Society. 1890.

Retterer, E. : 'Sur TOrigine et 1'Evolution de la Region ano-genitale des Mammiferes.' Journal de 1'Anatomie et de la Physiologic, xxvi. 1890.

Robinson, A. : ' Observations upon the Development of the Segmentation Cavity, the Archenteron, the Germinal Layers, and the Amnion in Mammals.' Quarterly Journal of Microscopical Science, xxxiii. 1892.

Schafer, E. A. : ' Quain's Anatomy.' Tenth edition, vol. i., part 1. 1890.

Strahl, H. : ' Zur Bildung der Cloake des Kaninchenembryo.' Archiv fur Anatomie und Entwickelungsgeschichte. 1886.

' Untersuchungen iiber den Bau der Placenta.' Archiv fur Anatomie und Entwickelungsgeschichte. 1889.

Tourneux, F. : ' Sur les Modifications que subit 1'CEuf de la Lapine pendant sa Migration dans 1'Oviducte, et sur la duree de cette Migration.' Comptes Rendus de la Societe de Biologic. Serie ix., tome 1. Paris. 1889.

Vassaux, G. : ' Recherches sur les premieres phases du Developpement de 1'CEil chez le Lapin.' Archives d'Ophthalmologie, viii. 1888.

Woodward, M. F. : ' On the Milk-dentition of Hyrax and of the Rabbit.' Proceedings of the Zoological Society. 1892.

Zimmermann, W. : ' Ueber einen zwischen Aorten- und Pulmonalbogen gelegenen Kiemenarterienbogen beim Kaninchen.' Anatomischer Anzeiger, iv. 1889.


Marshall (1893): 1 Introduction | 2 Amphioxus | 3 Frog | 4 Chick | 5 The Rabbit | 6 Human Embryo | Illustrations

Marshall AM. Vertebrate Embryology: A Text-book for Students and Practitioners. (1893) Elder Smith & Co., London.

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