Paper - Lectures on the early stages in the development of mammalian ova and on the differentiation of the placenta in different groups of mammals
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Robinson A. Lectures on the early stages in the development of mammalian ova and on the differentiation of the placenta in different groups of mammals. (1904) J. Anat. and Physiol. 38: 326-340.
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Lecture II On the Early Stages in the Development of Mammalian Ova and on the Differentiation of the Placenta in Different Groups of Mammals
By Arthur Robinson, M.D., Hunterian Professor.
(Plates XXXII. and XXXIII.)
The Placenta of the Pig
When the foetus of the pig has attained a length of 8.5 mm the surface of the chorion, except at the poles of the ovum, is covered with numerous small ridges which ﬁt into grooves on the surface of the maternal decidua. The ridges radiate from circular spots, which vary in number, as Sir William Turner pointed out, from twenty to thirty to the square inch. The chorionic ridges are irregular in size, both at this and at later stages, and the grooves on the surface of the decidua also vary in a corresponding manner, some being almost microscopical and others of considerable size (ﬁgs. 1 and 2). The adhesion between the trophoblast of the chorion and the uterine mucosa is never very firm, but it does not necessarily vary with the size of the ridges, being apparently closer in the intermediate than in the earlier or later stages. In all cases it is so slight that it is 11ot easy to retain the two membranes in apposition with each other, during their preparation for the microtome, but when this is successfully accomplished it is found that the surfaces of the chorion and decidua are closely applied to each other, and that both are covered by a very distinct epithelium. The sides of the smaller ridges are smooth, and devoid of offsets (ﬁg. 1), but from the sides of the larger ridges there are numerous secondary projections, which ﬁt into corresponding secondary sulci on the sides of the grooves in the decidua, in which the main ridges of the chorion lie (ﬁg. 2).
The epithelium on the surface of the decidua varies, but on the whole it is of the high columnar type, the cells in some places being narrower and more closely packed than the cells of the uterine glands, and in other places they are larger than the gland cells. The outer extremities of the decidual epithelial cells rest upon the subepithelial tissue, and are in close relation with the walls of numerous dilated capillaries which lie immediately external to them (ﬁgs. 2 and 4). The nuclei, which, as a rule, are round or of short oval form, lie near the bases of the cells, and the inner extremities of the cells are either very granular, and of very irregular contour, or they are bluntly rounded. When the inner extremities of the cells are very granular the boundary lines are obscured and the cells seem to blend together, but the inner extremities of the less granular cells are frequently separated from each other by distinct cleft-like intervals (ﬁg. 4).
The subepithelial tissue of the decidua is very vascular, and perhaps the most striking feature is the presence of numerous dilated capillaries which lie immediately beneath the epithelium, and ap parently in direct contact with the bases of its cells (ﬁg. 4).
External to the ‘vascular layer of subepithelial tissue is a layer of gland tubes running for the most part parallel with the surface, and having no communications with the sulci on the surface of the decidua, though some of the tubes lie in the intermediate ridges. As Sir William Turner has noted, the gland tubes pass obliquely or horizontally for a considerable distance, and their mouths open on the circular spots, from which the ridges and sulci. of the decidua radiate.
The trophoblast of the chorion in some places forms a nucleated syncytium in which no cell outlines are visible (ﬁg. 4); in other places it is divided into cell territories of columnar or cubical form, and both the outer surface of the syncytium and the outer extremities of the cells closely embrace the inner extremities of the -cells of the decidua, whilst from the cells, or from the syncytium, processes aregiven off which pass between the bodies of the decidual cells, extending, apparently, as far as the capillary layer of the subepithelial tissue. The connection, therefore, between the decidua and the trophoblast of the chorion is much more intimate than has generally been supposed, for the cells of the trophoblast are not only in apposition with the free surfaces of the cells of the decidua, but processes of the trophoblast cells, or of the trophoblastic syncytium, are wedged between the cells of the decidua, and I have little doubt that these processes are the cilium-like projections which Sir William Turner observed on the apices of some of the cells of a separated chorion.
The conditions above described are not only present in chorions associated with foeti of 8'5 mm. length, but they are also found after the foetus has attained a length of from 35 mm. 5 but, as a rule, when the foetus becomes larger the cells of the decidua decrease in size, and are more cubical and less columnar in form than in the earlier stages. Whether or not any other alterations take place in the later periods of development I am at present unable to say, as the material at my disposal is not yet prepared for cutting.
Since the uterine glands do not open into the sulci, in which the ridges of the chorion are lodged, but have their terminations in the small circular areas which were noted by Eschricht in 1837, as Sir William Turner has pointed out, and as, in the regions of the ridges and sulci, the trophoblast of the chorion and the epithelium of the uterus are in intimate apposition, it is clear that the secretion of the glands can only come into relation with the surface of the chorion in the regions of the small circular areas at the ends of the chorionic ridges.
It is also certain that the sulci and ridges of the decidua are interglandular, and are due to the increase of the interglandular portions of the mucosa, which has greatly extended the uterine surface and has pushed the oriﬁces of the glands together into small circular patches. It seems probable, therefore, that although the secretion of the glands is of considerable importance for the nutrition of the ovum in the stages which precede the intimate apposition of the trophoblast with the decidual epithelium, that it becomes less important afterwards, and that in the place of this indirect nutrition a process of direct transference from the cells of the mother to the cells of the trophoblast takes place. The latter process seems to be all the more probable inasmuch as the trophoblast cells contain numerous granules which behave in the same manner to staining reagents as the granules in the decidual cells, and many of these granules, as Kloster has shown, are of a fatty nature, and darken when treated with osmic acid. In addition to the utilisation of the gland secretion in the special areas, and the transference of material directly from the maternal to the foetal cells, it also seems probable that a certain amount of nutritive material may pass directly from the dilated capillaries into the decidual cells by means of the processes of those cells which pass outwards between the decidual cells till they come into relationship with the dilated subepithelial capillaries. . It is frequently stated that the surface of the chorion of the pig is covered with short villous processes ; this, however, is scarcely correct, and the structures noted as villi in sections are, for the most part, sections of the primary, secondary, or tertiary ridges of the chorion which are dipping into corresponding sulci of the uterine mucosa.
The Placenta of the Sheep
In the earliest stages, when the caruncles or rudiments of the maternal portion of the placenta are distinctly developing, the surface of the chorion remains smooth and devoid of villi or processes (fig. 5), but when the ovum has attained a length of several inches, and the caruncles are elevated above the general surface of the decidua, numerous small circular patches of rudimentary villi appear on the surface of the chorion. These circular patches correspond in number with the caruncles of the decidua, to which they are applied, and they constitute the cotyledons or foetal portions of the placenta. Each rudimentary villus consists of a surface layer of cubical cells, which may be blended into a syncytium, and it possesses a small core of foetal mesoderm.
The caruncles commence as proliferations of the interglandular tissue of the decidua in small circular areas. In the early stages each caruncle is a mushroom-shaped mass of very vascular subepithelial tissue, which is covered by a single layer of cubical uterine epithelial cells, ‘and it is surrounded by the mouths of numerous uterine glands, whose deep extremities converge beneath the caruncle, where they form a very evident glandular layer, which persists throughout all the subsequent stages (ﬁg. 5).
When they are ﬁrst evident the caruncles are raised little, if at all, above the general surface of the uterine mucosa, and their surfaces are smooth and devoid of pits or crypts. As development proceeds their subepithelial cores rapidly increase and become still more vascular, whilst their superﬁcial surfaces are depressed into shallow crypts, into which the chorionic villi are received. The diameter of the caruncles increases coincidently with their increase in height, and consequently the glands which lie beneath them become longer and assume a more horizontal position as compared with the earlier stages (compare ﬁgs. 5, 6, and 7).
None of the glands open on the surface of the caruncle or into its crypts. The caruncles are therefore interglandular in position and are of new formation, being produced by proliferation of the interglandular tissues, and this proliferation is associated with a great increase of the smaller blood vessels. As no glands open upon the surfaces of the caruncles, and as no degenerated glands are to be found in’ their substance, it is evident that in the first instance the proliferation of the connective tissues to which the formation of the caruncles is due must commence in a very limited area, that is, in one of the small intervals which exist between the various groups of gland oriﬁces, and as the proliferation increases, the mouths of the glands are gradually forced apart, until those which were at ﬁrst nearest the centre of the site of the commencing caruncle eventually open at its base.
As development proceeds the villi of the chorion become more massive, and the trophoblast on their surfaces thickens. At the same time the epithelium on the caruncle and in the crypts also thickens. This stage is succeeded by a period when the villi rapidly branch and become more slender, and their trophoblast is converted into a layer of columnar cells; but the cells of the villi do not appear to enter into such intimate relationship with the cells of the decidua as in the case of the pig. As the villi of each cotyledon lengthen and branch, their base of attachment to the chorion does not increase equally rapidly, consequently each group of villi forms a cauliﬂowerlike excrescencc which is attached to the surface of the chorion by a relatively narrow stalk.
Coincidcntly with the growth and branching of the villi of the cotyledon the crypts of the caruncle, in which they are embedded, become deepened and divaricated, until, ﬁnally, the caruncles become bulb-like prominences. The interior of each bulb-like caruncle consists of a large number of complicated canals corresponding with the branches of the villi which they contain. These canals are lined with a columnar epithelium, which rests upon a base of very vascular connective tissue, and the margin of the hollow bulb closely embraces the stalk of the cotyledon, and round it the epithelium lining the canals of the caruncle becomes continuous with the epithelium on its outer surface.
The extraordinarily complicated interweaving of the villi and of the cotyledon and the septa of the caruncle makes it difficult to believe that when the villi are withdrawn from the caruncles, at birth, they do not carry with them a certain amount of the maternal cells. Hitherto I have not had the opportunity of examining the cotyledons of a freshly-shed chorion, but it is well known that a certain amount of blood is lost by the mother at the period of birth. Presumably, therefore, some of the maternal vessels are opened by the tearing of the septa of the caruncle, and Sir William Turner discovered cells similar to the cells of the caruncle on the surfaces of the villi of the cotyledon which he examined. To make the proof absolute it would be necessary to examine the caruncles directly after birth, and the opportunity of doing this has not yet presented itself‘.
It is certain, however, that the caruncles of the sheep are new formations, and that in them the cells of the foetal trophoblast and the cells of the maternal decidua are in close apposition with each other, but that at present there is no evidence of that intimate intermingling of the trophoblast cells with the cells of the decidua which is so striking a feature of the placenta of the pig. Further, in the sheep, instead of a large series of ridges covering the whole surface of the chorion, and interlocked with the corresponding grooves on the decidua, as in the pig, there are a number of circular patches of much—branched villi, which vary in number from 60 to 100, which are scattered irregularly over the surface of the chorion except upon its poles.
In placentae of this formation nutriment may pass to the ovum (1) by secretion from the uterine glands which reaches those parts of the chorion, relatively large in extent, which are not engaged in the formation of cotyledons; (2) by transmission of nutriment directly from the cells of the crypts to the cells of the villi, and this probability is strengthened by comparison with the pig, for in the latter animal it seems certain that granules which appear in the decidual cells are transferred directly to the trophoblast, and are passed by it to the remainder of the ovum and the embryo. Indeed, from Kloster’s observations it seems probable that amoeboid cells carrying blood pigment may pass between the decidual cells into the trophoblast, and so furnish the iron necessary for the embryo. If the maternal epithelium disappears in the later stages, as Frankel asserts, the transmission of nutriment directly from the decidua to the foetal tissues will be greatly facilitated.
The Placenta of the Cat
About the twelfth day of gestation, and before the amnion folds have formed, a broad zonular band of the trophoblastic portion of the chorion is intimately attached to the maternal mucous membrane. The band runs round the central part of the citron-shaped ovum, the poles of which are free and devoid of ridges or villi. On the antimesometrial side of the uterine cavity the zonular band of adhesion is cleft into two lateral parts, and in the interval between them lies the embryo, and the amniotic section of the ovum which has not yet closed in over the embryo. The latter, therefore, and the amniotic area around it are separated from the surface of the uterus by a fluid—filled space, and they are bulged towards the interior of the ovum, in spite of the fact that, in the ordinary position of the mother, they lie on its ventral or lower surface, and are not, therefore, carried into the interior of the ovum by their own weight.
As development proceeds the margins of this space in the zone of attachment are approximated to each other, growing inwards over the surface of the uterine mucosa. Consequently the outer margins of the amniotic area are also approximated, and ﬁnally fused together, simultaneously with the completion of the zonular band of adhesion. lmmediately afterwards the amnion separates from the chorion, and passes, together with the embryo, further into the interior of the ovum.
At the twelfth day the zonular band of trophoblast which is adherent to the uterine tissues consists of a layer of nucleated protoplasm, in which the nuclei form one or two rows, and the layer tends to be divided into distinct cell territories in certain parts of its extent.
The mucous membrane of the uterus immediately around the ovum is thickened, and consists of a vascular connective tissue interspersed with numerous dilated glands. In the regions at the poles of the ovum, where the ovum and the uterus are not attached together——that is, to either side of- the zonular band—the tortuous glands open on the surface of the mucosa, and their epithelium is continuous with that covering the inner surface of the uterus in the interglandular areas. In the region of the zonular placental band the condition of the mucosa is more profoundly changed, and in this area two regions are to be distinguished—that opposite the embryo and the amnion, where attachment is not yet completed, and the zonular band, where attachment has already taken place. In both areas the outer part of the decidua contains the outer extremities of the glands, which differ little if at all from the corresponding parts in the non-placental region. Further inwards is a layer of large cell-lined spaces, obviously due to localised dilatations of the glands, the spongy layer of the decidua. Still more internally the glands are less dilated, and, therefore, the interglandular tissue is relatively greater in amount. This area, which constitutes the compact layer, is a comparatively thin stratum lying immediately adjacent to the surface of the decidua. In many places over the amnion and embryo the compact layer is deﬁcient or extremely thin, and the dilated portions of the glands are merely roofed over by their own epithelium, which completely separates their cavities from the cavity of the uterus, or through which they open by relatively small apertures, whilst in other places somewhat narrow channels pass from the dilated parts of the glands through the compact layer to the surface, which is covered by a layer of ﬂattened cells. These ﬂattened cells on the surface of the decidua, opposite the embryo and the amniotic portion of the ovum, appear to be continuous with the columnar epithelium lining the glands, and they probably represent an epithelium in the process of atrophy.
In spite of statements to the contrary, I cannot satisfy myself that in the cat there are any crypt-like depressions of the mucous membrane which are not in continuity with the gland tubes in the more external part of the mucosa, and therefore I am forced to the conclusion that no such crypts are formed in the area over the embryo and amnion. In the region in which adhesion has already taken place none of the glands or crypt-like dilatations of the glands communicate with the surface; on the contrary they are separated from it by a layer of compact connective tissue in which are many capillaries, and to which the trophoblastic cells of the chorion are intimately attached, the maternal epithelium having entirely disappeared. Here and there, it is true, small villous processes of the chorion project into the mucosa, piercing the compact stratum and coming into direct relationship with the epithelium of the crypt-like dilatations of the glands, but there is no evidence that these processes have passed into the mouths of newly-formed crypt-like dilatations of the mucous membrane of the uterus.
In the outer part of the compact stratum of the decidua, as before mentioned, there are numerous dilated capillary vessels, and the outer walls of many of these vessels are in direct contact with the foetal trophoblast, nothing but the endothelium of the vessel wall intervening betweenthe maternal blood and the trophoblastic protoplasm, which is of synctial character, no cell outlines, as a rule, being visible in its substance in these regions.
As gestation proceeds the villous processes of the chorion grow longer, and penetrate further and further into the decidua, in which the glands recede further and further from the surface, whilst they undergo numerous and complicated alterations. The lumina of some of the glands and spaces areobliterated, and the surrounding epithelium degenerates and is transformed into strands of granular nucleated protoplasm. This probably serves as pabulum which is absorbed by the trophoblast of the advancing chorionic villi. The epithelium of other obliterated spaces proliferates and appears to take part in the formation of the interglandular tissue into which the chorionic villi are extending. In still other spaces, and more especially in those against whose outer walls the apices of the invading villi have encroached, the epithelium of the inner wall of the space which is adjacent to the villus proliferates rapidly and then breaks down into a granular nucleated detritus, which appears to be absorbed by the foetal trophoblast, granules appearing in the trophoblastic protoplasm, which stain similarly to those in the glandular detritus.
In still later stages the villi of the chorion replace all the outer portions of the decidual tissue except the maternal blood vessels. The latter pass outwards between the glands in the deeper parts of the decidua and between the masses of detritus derived from degenerated glandular epithelium, and entering the intervals between the trophoblast of adjacent villi they continue inwards to the inner surface of the placenta, where they enter terminal dilatations which are also surrounded by the foetal trophoblast, the latter intervening between the walls of the maternal vessels and the foetal mesoderm which covers the foetal surface of the placenta and extends outwards, forming the cores of the villi. The maternal vessels as they run inwards are much convoluted, therefore they are out many times in vertical sections of the placenta taken at right angles to the surface of the uterus. VVhen such sections are examined with the higher powers of the microscope the ultimate structure of the placenta becomes evident (ﬁg. 14).
The walls of the maternal vessels are formed by a single layer of enlarged endothelial cells. Immediately outside the endothelium there is either a layer of large cells, or a syncytium of nucleated protoplasm, and this in its turn is surrounded either by a distinct layer of cells or in many places by a second syncytium, which is more or less clearly marked off from that immediately around the endothelium by a boundary line. On the outer side of the foetal ectoderm layers is the foetal mesoderm. These general characters are not disputed by any of the later observers who have examined the cat’s placenta, and the conditions are essentially the same in the dog, but there are two directly opposite views regarding the nature of the nucleated syncytium, or layer of large cells, immediately outside the endothelium of the maternal vessels. According to one View it is of maternal origin, and according to the other it is foetal and constitutes the outer layer of the trophoblast of the chorion. The observers who believe it to be of maternal origin are again divided amongst themselves, some ascribing its origin to the maternal uterine epithelium and others to the subepithelial tissues. It would serve no good purpose to discuss this difference of opinion at this point, but it may be necessary to return to it when we have considered the other forms of placenta and so have obtained further evidence from other sources. If, however, it is admitted that the layer of syncytium or cells immediately adjacent to the endothelial walls of the maternal vessels is foetal, as Duval asserts, then it may represent the plasmodiblast layer of the bats’ placentee, whilst the more external foetal ectoderm would then correspond with the cytoblastic layer of the bats’ chorion.
In still later stages the plasmodiblastic layer disappears, and the cytoblastic layer, which is undoubtedly foetal, but which may be either syncytial or cellular, lies in direct relation with the endothelial walls of the maternal vessels.
The Placenta of the Ferret
After the segmentation of the ferret’s ovum is completed the blastocyst, which results, soon becomes didermic. The inner layer of the vesicle is formed by ﬁat entodermal cells, and the outer wall consists of ectoderm, which soon becomes separated into three distinct areas. First, the embryonic area, which lies opposite the antimesometrial border of the uterine cavity. In this area the cells are of columnar form. Second, the amniotic area immediately around the embryonic area. In the amniotic area the ectodermal cells are ﬂattened squames. The third area is the chorionic area, and it includes all the remaining surface of the ovum, but the trophoblastic ectoderm which covers its surface has not the same characters in all parts. Over the poles, where the ovum is in relation with the portions of the uterine canal situated above and below the trophoblastic ectoderm, and along the mesometrial border of the uterus, it is either ﬂat or of a low cubical form, but over the remainder of the chorionic surface the ectoderm tends to assume a low columnar form, and in many places the cell outlines are lost and a syncytium is formed (ﬁg. 8). At a slightly later period the most interesting character of this part of the chorionic area is the presence of small nodular outgrowths on the surface of the trophoblast (fig. 9). These nodules consist of granular nucleated protoplasm, which not only stains differently from the adjacent trophoblastic ectoderm, but is also sharply marked off from the latter by a ﬁne boundary line.
Some of the nodular processes project into the dilated mouths of uterine glands, but these are the exceptions (ﬁg. 9), and by far the greater number abut against the epithelium between the oriﬁces of the glands, destroy it, and enter the subjacent subepithelial tissue (fig. 10). At this period also the mouths of many of the uterine glands become closed by the proliferation of the uterine epithelium by which they are lined.
At a slightly more advanced stage of development, whilst the neural groove of the embryo is still unclosed, the condition both of the chorion and that of the decidua is considerably altered. The tropho— blastic epithelium of the chorion now forms a continuous syncytium, in which the nuclei lie frequently in two planes, but which is not easily separable into two layers, and this syncytium is closely connected with the surface of the decidua, from which the maternal epithelium has entirely disappeared. In the subepithelial tissue of the uterus, which has greatly increased in amount, numerous dilated capillaries have appeared, many of which are in direct contact with the trophoblastic epithelium (fig. 11), as in the corresponding stage of placental formation in the cat. The mouths of the glands which lie in those parts of the walls of the uterus with which the trophoblast is united are closed, and the epithelium has either disappeared at their inner ends or it has thickened and assumed a syncytial character.
Along the mesometrial border of the uterus at this stage the epithelium of the glands and the small interglandular portions of the uterine surface is enlarged, the inner ends of the cells being especially swollen. In the interglandular areas the apices of the swollen cells are in contact with the trophoblastic syncytium, but there is no fusion between the two layers.
The most striking changes, however, are seen along the antimesometrial border of the uterine cavity opposite the embryo and the amniotic portion of the ovular surface. Here the maternal epithelium has entirely disappeared from the uterine surface, although the latter is not in contact with any portion of the surface of the ovum. The mouths of all the glands which were open in the preceding stage in this area are now closed. The inner ends of the glands terminate in columns of cells which are evidently produced by the proliferation and fusion of the epithelium of the walls of the glands, and these columns are separated from the surface of the uterus by a fairly thick layer of vascular connective tissue, which terminates internally in the irregular and epithelium-denuded-surface. Over this denuded surface the chorion gradually extends inwards, carrying the amnion folds with it until the latter meet, fuse together, and ﬁnally separate from the chorion, but before this separation is accomplished the allantois has attained a connection with the inner surface of the chorion 3 therefore the embryo still retains its direct connection with the chorionic surface of the ovum.
During the next few days villous processes of the chorion extend further and further into the substance of the decidua, and at the same time the cavities of the glands come to lie at a greater distance from the surface, but they occupy relatively the same positions with relation to the apices of the villi that they did at the earlier periods that is, the outer walls of the closed and dilated tubes are comparatively close to the apices of the longest villi, and their epithelium still shows signs of active proliferation and marked degeneration. Here and there the apices of the longest villi lie in direct contact with the degenerated epithelium of the uterine glands, but in other places they are separated from it by a layer of interglandular tissue.
Whilst the primary villi have been increasing in length the intervillous areas of the decidua have also grown, and into these areas secondary and tertiary villi of the chorion have begun to penetrate (ﬁgs. 12 and 13). The tissue of the intervillous areas of the decidua appears to be formed partly by proliferating connective tissue cells, and partly by altered epithelial cells produced by the proliferation of the cells of the uterine glands, some of which appear to retain their vitality and to take part in the growth of the decidua, whilst others undergo degeneration and form cords and strands of degenerating epithelium in the intervillous areas.
The blood vessels of the superﬁcial layers of the decidua are still numerous, and many of them lie directly in contact with the trophoblastic epithelium which covers the internal surface of the intervillous areas. There are also many lymphatic spaces present in all parts of the decidual tissue, the majority of them running parallel with its uterine surface. Up to this period, about the ﬁfteenth day, there has been no diminution of the thickness of the layer of uterine glands, but, on the contrary, an increase, and at the end of this period an effusion of blood between the chorion and the decidua commences. This effusion of maternal blood from ruptured blood vessels of the decidua is a common phenomenon both in carnivorous and other placentae, and it occurs in different situations in the different groups of the carnivora. In the cat it is irregular both in position and in amount. In the dog it occurs regularly along the margins of the placental zone, and in the ferret it is always found at the_antimesometrial border of the uterus, where the placental band was last completed, and it cuts the band into two lateral discs.
Whether the blood at the anti-mesometrial border of the uterus accumulates in the ﬁrst instance in enormously dilated capillaries or not—and about this there is some doubt——it eventually ruptures the walls of the vessels, and, reaching the surface of the decidua, it lifts the trophoblast of the chorion from the decidual tissue and forces it in the form of irregular pouches towards the interior of the ovum. When this has occurred, and before the effused corpuscles of the blood have broken down, many of them are taken bodily into the interior of the cells of the trophoblast, which, in this region, have again become distinctly separated from each other, and after degeneration .of the effused blood has occurred, masses of blood pigment are seen in the interiors of the trophoblastic cells.
In the succeeding stages the villi of the chorion increase in length, and they press outwards against the layer of glands and degenerating gland epithelium, which now becomes reduced in thickness. At the same time offsets from the sides of the 'vi1li penetrate the intervillous portions of the decidua and still further break it up, until ultimately the foetal and maternal tissues together form a series of irregular and interlocking lamellae. The lamellae are of two kinds :—(1) lamellae of foetal mesoderm, and (2) lamellaa formed by two layers of syncytium or a layer of cells and a syncytium enclosing maternal vessels. Thus a condition is attained which is practically similar to that noted in the placenta of the cat. The walls of the maternal vessel are formed by enlarged endothelial cells, which are closely surrounded by a layer of large cells, which merge in some specimens into a syncytium, and the latter is, in its turn, enclosed by a second layer of syncytium or by a layer of large cubical cells, which are in relation externally with the vascular foetal mesoderm.
In still later stages the outer syncytium—that adjacent to the maternal vessels, which possibly corresponds with the plasmodiblastic layer of Van Beneden—disappears, and the maternal blood is then separated from the foetal blood by the endothelial walls of the maternal and the foetal vessels and by a single layer of ectoderm, which may be either syncytial or cellular in character, and which possibly correspond with Van Beneden’s cytoblast.‘
In the ferret, as in the cat, nutriment is conveyed to the embryo partly by means of interchanges between the fmtal and maternal blood streams through the foetal ectodermal layer or layers, and at the same time effused maternal blood is taken into the interiors of the foetal chorionic cells, where it is broken down, and the products which result are transmitted to the embryonic tissues. It is probable also that the non-placental ectoderm at the poles of the ovum absorbs the secretion which is poured out by the enlarged uterine glands in the immediate neighbourhood.
The Placenta of the Leopard
Of the placenta of this animal I have only been able to obtain a specimen which was believed to be within a short time of the full term, and it is worthy of note merely because, so far as I know, the minute features of the placenta of this animal have not hitherto been described. The placenta is a zonary placenta, not dissimilar to that of the cat in naked-eye appearance and in section. It consists of an external layer of closed and dilated glands, on the inner walls of which the epithelium is proliferating and degenerating, and this is succeeded by a thick stratum of maternal blood vessels intermingled with foetal villi which run for the main part at right angles with the surface. The maternal vessels, as in the cat and the ferret, are extremely sinuous, and each is, therefore, out many times and in many planes in each section of the decidua. Many of the maternal vessels are distended with blood, and the endothelial cells which form their walls are expanded and ﬂattened. Outside the endothelium there is a single layer of nucleated syncytial tissue, and this is bounded externally by the vascular foetal mesoderm. The structure is therefore similar to that met with in the cat and the ferret in the later stages.
- 1 At the present moment I am not prepared to assert that the layer of large cells which lies between what is undoubtedly foetal ectoderm and the maternal blood vessels, and which I have suggested may represent the plasmodiblast, is foetal. Its history is diﬂicult to follow, and I am accepting for the moment Duval’s view, which is based upon his observations on the dog and cat, and which is opposed to the views of Bonnet and Strahl. I hope to enter more fully into this subject in a future communication.
The Placenta of the Rat and the Mouse
The placentae of the rat and the mouse differ in many essential respects from the placentae previously considered. In the pig, sheep, cat, and ferret, the placental area of the chorion is lined, in the early stages, by the entoderm, subsequently by somatic mesoderm, and ﬁnally the allantois fuses with the somatic mesoderm ; and in transverse section of the placental area the layers met with from without inwards are the trophoblast of the chorion, the fused somatic and allantoic mesoderm, and the allantoic ' entoderm. In these animals, therefore, the placenta in its early stages is an omphalic or vitelline placenta, but, after the extension and cleavage of the mesoderm, by which the entoderm of the yolk-sac is separated from the inner surface of the trophoblast, and the simultaneous fusion of the allantois with the inner surface of the somatic mesoderm, the placenta becomes an allantoic placenta. The extension and cleavage of the mesoderm takes place from the embryonic area outwards, and the cleavage especially is a relatively slow process, therefore there exists, for a considerable time, a double condition of the placental area of the chorion. Over the greater part the mesoderm which has extended between the entoderm and the ectoderm is still uncleft, and the placenta is an omphalic placenta, whilst over the smaller area the yolk-sac is separated from the chorion by the extra-embryonic portion of the coelom, and in this region the allantoic mesoderm has fused with the somatic mesoderm on the inner surface of the chorion, therefore the latter portion of the placenta is allantoic. The allantoic portion gradually increases as the omphalic decreases, until, eventually, the allantoic completely replaces the omphalic placenta.
In the rat and the mouse, however, the mesoderm never extends completely round the ovum, therefore the yolk-sac in these animals enters into the formation of a strictly omphalic placenta, consisting on the one hand of the maternal decidua and on the other of foetal trophoblastic ectoderm lined internally with entoderm. This portion of the placenta persists throughout the greater part of the intra-uterine development, and it is upon it that the nutrition of the embryonic and extra-embryonic portions of the ovum appears to depend for a relatively prolonged period, for the allantoic placenta forms tardily and in a very peculiar manner. I
Whilst the ovum is still a blastula it enters a crypt in the decidua on the anti-mesometrial border of the uterus. There it expands into a spherical vesicle, and, as the sides of the blastula come into contact with the sides of the crypt, the epithelium on the latter disappears. As development proceeds the ovum assumes a cylindrical form ; one pole is turned towards the blind or anti-mesometrial end of the crypt, in which the maternal epithelium proliferates, until it obliterates the cavity, and then it becomes absorbed, or at all events it disappears, its place being taken by a vascularised tissue. The opposite or mesometrial end of the crypt remains in free communication with the uterine cavity for some time, but ﬁnally it also becomes closed after its epithelium has degenerated. In the meantime, however, a mass of trophoblastic ectoderm has grown from the mesometrial pole of the ovum into the corresponding segment of the crypt. At ﬁrst this mass is more or less cylindrical in form, but it soon becomes conical, its base resting on the mesometrial pole of the ovum where it covers the border of an invaginated yolk-sac, and becomes continuous with the trophoblast on the outer surface of the ovum, and also with an internal tube of trophoblastic cell which has been invaginated towards the interior. The sides of the conical mass fuse with the maternal decidua, from which the maternal epithelium has entirely disappeared, and in the interior of the mass a number of irregular spaces appear which extend to the surface, where they communicate with the cavities of the maternal capillaries, from which they receive maternal blood. In the meantime the trophoblast on the outer surface of the yolk-sac has become so intimately blended with the decidua that it is impossible to say where one ends and the other begins, but it is obvious that the maternal blood has entered spaces in the trophoblast, or the trophoblast has disappeared, for the blood can be traced into close contiguity with the outer surfaces of the entoderm, or, at all events, with a membrana hypoblastica which lies immediately outside the entodermal cells. Under these circumstances there is no difficulty in appreciating how readily nutriment may pass from the maternal blood to the entoderm of the yolk-sac, but the part played by the blood in the conical plug of trophoblast is somewhat difﬁcult to determine, unless its purpose is merely to provide nutriment which will facilitate the further growth _of this mass, for the base of the mass is separated from the embryonic area by a considerable space, which is subsequently divided into the amniotic cavity and the trophoblastic cavity, which themselves become separated by the coelom. At a later period, as the coelom expands, the internal trophoblast is evaginated against the base of the trophoblastic cone, and it is not until after several mesodermal somites have formed in the embryo that the allantoic mesoderm attains a connection with the somatic mesoderm on the base of the trophoblastic cone (ﬁg. 15).
The allantois in the rat and mouse is a solid mass of mesoderm absolutely devoid of an entodermal cavity at any period of its existence. It grows out from the posterior end of the embryo, through the extra-embryonic coelom, as a club-shaped mass of mesoderm, and ultimately fuses with the evaginated layer of internal trophoblast (03/, ﬁg. 15) at the mesometrial pole of the ovum. Thus it becomes indirectly associated with the base of the conical mass of external trophoblast which covers the mesometrial pole, in the spaces of which maternal blood is already circulating. In the meantime the decidual tissue which has formed around the ovum on the mesometrial border of the uterus has enlarged, until its mesometrial surface has fused with the opposite wall of the uterine canal, the cavity of which is now entirely obliterated in the region of each developing ovum. After the allantois has fused with the chorion the ovum soon loses its cylindrical form, ﬁrst becoming spherical and then ovoid, the long axis of the oval coinciding with the long axis of the uterine canal; and whilst these alterations of form are taking place changes are occurring both in the allantoic portion of the placental area and in the relation of the decidua to the walls of the uterine canal.
The changes which occur in the allantoic portion of the placental area are of a twofold character, changes associated with the relations of the trophoblast to the maternal tissues and to the foetal mesoderm, and changes associated with the relation Of the entoderm to the placenta.
After the union of the allantois with the chorion the mass of external trophoblast at the mesometrial pole of_ the ovum rapidly increases in thickness, and it spreads out laterally, whilst the spaces in its interior which contain maternal blood increase in number and complexity. At the same time villous projections of the internal trophoblast containing cores of foetal mesoderm extend into the external trophoblast (ﬁgs. 16 to 18). Eventually the cells of the internal trophoblast blend with the syncytium of the external trophoblast, and the foetal placenta, which now forms a discoid mass, consists of foetal trophoblast which is intimately connected externally with the decidua. The capillaries of the latter are continuous with the spaces of the trophoblast, and the blood-laden trophoblast is itself penetrated and cleft into segments by villous processes of the foetal mesoderm bearing foetal vessels in their interiors. When this condition is achieved the maternal blood in the placenta is separated from the foetal blood by a layer of trophoblast and the endothelial wall of the foetal vessel—that is, by two layers of foetal tissue.
The changes of relationship between the entoderm and the placenta which occur during the period under consideration are simple, but extremely suggestive of important functions. At the commencement of the period the outer wall of the yolk-sac, at the mesometrial pole of the ovum, lies beneath the outer margin of the base of the placental cone of trophoblastic ectoderm, and the circular border where the outer wall blends with the invaginated portion of the sac embraces the stalk of allantoic mesoderm which connects the embryo with the allantoic placenta. As the development proceeds, ﬁnger-like processes from this circular mesometrial border of the yolk-sac penetrate the stalk of the placenta and acquire a close relationship with the walls of the placental vessels (ﬁg. 18, D173). Moreover, this peculiar extension of the yolk-sac entoderm into the allantoic placental region occurs simultaneously with the gradual cessation of the circulation of maternal blood in the decidua of the omphalic placental area, for as the processes extend into the stalk of the allantoic placenta, the decidua gradually separates from the antimesometrial border and from the sides of the uterus, and simultaneously in the separated part of its extent it becomes much thinner and less vascular than in preceding stages} Finally the whole of the latter portion of the decidua, together with the corresponding part of the yolk-sac entoderm, disappears, and the cavity of the yolk-sac becomes continuous with the cavity of the uterus. At the same time the continuity of the latter cavity, which was broken when the decidual tissue which formed on the antimesometrial border of the cavity fused with the mesometrial wall, is reestablished. When the condition above described is attained the foetus is attached to the discoid placenta on the mesometrial side of the uterus by an allantoic stalk, and, hanging by this stalk, it projects into the uterine cavity surrounded by its amnion and by the inner wall of the yolk-sac, on which the epithelium retains its columnar character. Speaking generally, the conditions thus established are retained till birth, except that, as my specimens of older placentae lead me to think, the processes of the yolk-sac which enter the allantoic stalk and the base of the allantoic placenta undergo atrophy before the termination of the gestation.
- 1 This separation is indicated as having already occurred in ﬁg. 15 3 in reality it takes place at a later period than that depicted in the ﬁgure.
In the rat and the mouse, therefore, a single discoid allantoic placenta is formed for each embryo, and it consists, with the exception of the maternal blood in its spaces, entirely of foetal tissues, foetal trophoblast, and foetal mesoderm. It differs, therefore, from the placentae of the carnivora we have considered, not only on account of its form, but also because there is no maternal epithelium, either glandular or derived from the surface, in its substance, and because, for a time at least, processes of yolk-sac entoderm enter into it.
Some years ago I drew attention to the peculiar entrance of yolksac entoderm into allantoic placenta, and suggested that it was associated with the absence of entoderm in the allantois ; and at a later period Duval, working upon the development of the guinea-pig, pointed out that the placental formation, in that animal, tended to support the suggestion I had made. He found that in the guineapig, as in the rat and mouse, the allantois was devoid of entoderm, and that in it also yolk-sac entoderm entered the allantoic placental area, not, however, on its foetal surface, as in the rat, but on its maternal surface, cutting the connections between the foetal and maternal tissues into a number of bands, which serve in the later stages to unite the foetal portion of the placenta with the decidua.
What function this placental entoderm subserves I have not yet been able to discover; that it is not a necessity in all animals is certain, for in the higher forms practically no entoderm enters the allantoic mesoderm, and no yolk—sac entoderm passes into the placental area. Moreover, in the rat and mouse it gains association with the allantoic placental tissues shortly before the greater part of the outer wall of the yolk-sac disappears ; thus any secretion it may pour into the upper part of the yolk-sac cavity would pass into the uterine cavity. On this account I am rather inclined to look upon any entoderm in the allantoic placental region as not necessarily an arrangement for foetal nutrition, but more probably as an adaptation for foetal excretion, and it seems not improbable that allantoic entoderm, when it is present in the placental area, may serve a similar purpose.
The general mode of formation and the general characters of the placenta in the mouse and the rat show that nutriment is conveyed to the embryo by means which differ essentially in the early stages from those met with in the ungulates and carnivora, and the most striking difference is the entire absence of glandular secretion, from which the surface of the ovum is entirely excluded at an early period, and the more intimate association of the foetal blood vessels and the foetal entoderm with the maternal blood.
It is interesting, however, to note that in the rat and the mouse two layers of foetal ectoderm intervene between the foetal blood vessels and the maternal blood for a considerable period, an outer syncytial layer corresponding with Van Beneden’s plasmodiblast and an inner trophoblastic layer deﬁnitely cellular at some periods and corresponding probably with Van Beneden’s cytoblast. In all probability the two layers correspond with the two layers of ectoderm met with in the carnivora, and, as in the latter animals, so also in the rat and the mouse they are ultimately reduced to a single layer, which probably represents Van Beneden’s cytoblast in both groups of animals.
Explanation of Plates XXXII and XXXIII
AM. Allantoic mesoderm. FM. Foetal mesoderm. AS. Allantoic stalk. IT. Internal trophoblast. C’. Coelom. MB. Maternal blood vessel. OR. Caruncle. MM. Mucous membrane. 01’. Cotyledon. PL. Plasmodiblast. Cy. Cytoblast. SM. Somatic mesoderm. D. Decidua. Spm. Splanchnic mesoderm. DE. Degenerating Epithelium. U0. Uterine cavity. DYs. Diverticulum of Yolk-sac. UE. Uterine epithelium. ET. External trophoblast. UG'. Uterine glands. FB. Foetal blood vessel. UM. Uterine muscle. FE. Foetal ectoderm. YS. Yolk-sac.
Figs. 1 and 2. Diagrams representing two stages in the formation of the placenta of the pig.
Fig. 4. A portion of a pig’s placenta more highly magniﬁed than ﬁg. 2, showing the relation of the foetal ectoderm to the maternal tissues.
Figs. 5, 6, and 7. Diagrams representing three stages in the formation of the placenta of a sheep.
Figs. 8 to 13. Diagrams representing different stages in the formation of the placenta of a ferret.
Fig. 14. Diagram representing a portion of the placenta of a cat.
Figs. 15. to 18. Diagrams representing stages in the formation of the placenta of a rat. Joum. of Amt. and Physiology, April 1904.] [PLATE XXXIL
Cite this page: Hill, M.A. (2021, May 18) Embryology Paper - Lectures on the early stages in the development of mammalian ova and on the differentiation of the placenta in different groups of mammals. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Lectures_on_the_early_stages_in_the_development_of_mammalian_ova_and_on_the_differentiation_of_the_placenta_in_different_groups_of_mammals
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