Paper - On the question of the interpretation of the structural features of the early blastocyst of the guinea-pig (1928)
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Wilson JT. On the question of the interpretation of the structural features of the early blastocyst of the guinea-pig. (1928) J Anat. 62: 346-358. PMID 17104199
|blastocyst of the guinea pig.
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On the Question of the Interpretation of the Structural Features of the early Blastocyst of the Guinea-pig
By J. T. Wilson
Professor of Anatomy, University of Cambridge
Dr Norman Macuaren has recently made public some of the results of his reinvestigation of early phenomena of the development and implantation of the blastocyst of Cavia(1). The nature of his conclusions has induced me to re- examine critically the statements of various observers respecting the structural characters of the blastocyst of this Rodent, during the earlier phases of its development.
Since the appearance of Bischoff’s monograph on the subject in 1852 (2) a number of workers have made contributions to the problem but their con- clusions have been more or less discordant.
For the purposes of this paper it is unnecessary to review in detail the literature of the subject. The previous literature of early Rodent development has been analysed by Selenka (8) and, after him, in greater detail by Duval (4), in their now classical memoirs. Comprehensive lists of references to the later literature are available in Hertwig’s Handbuch (5) and in the quite recent work of Grosser ( (6), 1927).
Duval has pointed out that, in a communication appearing in September, 1882, Fraser (7) was the first to recognise that “inversion of the germ layers” is a feature common to various other Rodents besides the Guinea-pig. The same conclusion was reached independently and almost simultaneously by Selenka (3) in a publication which appeared a few months later.
To the latter author we also owe the knowledge of the absence in Cavia of a completed entodermal yolk-sac layer.
Thus far no general explanation of the phenomena of inversion had been forthcoming, but the solution of this general problem was fully worked out in Selenka’s subsequent memoirs of 1883 and 1884.
This solution, in the case of the Mouse and Rat, was fully confirmed by the later studies of Duval and has ever since held the field so far as the latter types are concerned.
The condition in the Guinea-pig, however, shows some divergence from the otherwise closely related type of the Muridae.
As already stated, Selenka found that in Cavia a complete vesicular, entodermal, yolk-sac wall is not constituted. Only a proximal “visceral” layer of (“inverted”) entoderm covering the central ectodermal cylinder is present. Later this becomes a conspicuous columnar layer. No one has succeeded in demonstrating the existence, at any period, of a distal or “parietal” ento- dermal layer representing an entodermal lining of the parietes of the cavity within which the amnio-embryonic cylinder is inverted.
2 Originally presented at the Joint Meeting of the Société des Anatomistes and the Anatomical Society of Great Britain and Ireland, held in London, April, 1927. Structural Features of Early Blastocyst of Guinea-pig 347
Even in the Muridae such a distal entodermal layer is very inconspicuous and sometimes more or less imperfectly formed.
Nevertheless in them it is for a time clearly recognisable as a cellular lining to “‘Reichert’s membrane,” as Selenka’s and Duval’s figures show. Its presence is indeed easily verifiable at any time in suitable sections. But it appears to be totally absent in Cavia.
There can be little doubt that this entodermal deficiency in the latter case must be correlated with the fact that in this type no Reichert’s membrane is formed. The presence of any other representative of the original trophoblastic wall of the blastocyst is at best so difficult to establish that its real existence is strenuously denied, as we shall see, by some observers.
Selenka, however, quite definitely maintained the objective reality of such an outer layer of (trophoblastic) ectoderm (“‘hinfalliges Ektoderm,” auct.). In various figures of Taf. x1 of his 1884 memoir (“‘ Die Blatterumkehrung,” etc.) he shows it as a quite recognisable, though faint and impermanent, layer.
A like view was adopted by Duval although in this instance it was un- supported by other than schematic figures.
Selenka’s representation of the facts seems to have been accepted by such later authorities as Hertwig (loc. cit.) and by Grosser(6) who (1909) copies Duval’s schemata, or (1927) the schemes of Pytler and Strasser (8) which are evidently founded on Duval.
On the other hand Graf Spee(9), in his important monograph on the implantation of the ovum in the uterine wall in the Guinea-pig, has given expression to opinions entirely inconsistent with those of Selenka and Duval on this question. He emphatically rejects the view that there is present at any time in the implanted ovum of the Guinea-pig any such outer ectodermal wall of the blastocyst, transient or otherwise, as that represented by Selenka and Duval.
His explicit opinion to the contrary may here be quoted literatim: “Zu dieser Ansicht bin ich durch das Studium auch der spateren Stadien immer wieder zuriickgekommen und betone dies hier nur deswegen, weil Selenka und nach ihm Duval von einer dem Ei zuzurechnenden verganglichen Deckzel- lenschicht berichten, wie sie auch fiir das Ei der Ratte und Maus von diesen Autoren beschrieben wird, und die wie ein weiter Sack den gréssten Theil des Eies einhiillen soll. Eine Deckzellenschicht dieser Art existirt beim Meerschweinchen ganz bestimmt nicht.”
This decisive divergence from the widely accepted scheme of Selenka and Duval acquires special importance in view of the fact that this particular contribution of Graf Spee to knowledge of the early development and implantation, in utero, of the ovum of the Guinea-pig has remarkably influenced subsequent embryological theory on the subject of mammalian implantation.
It is to me very surprising that several later writers (cf. Grosser, 1927), whilst professing to follow Selenka and Duval in their recognition of a transient ectodermal (trophoblast) wall of the blastocyst (“hinfalliges Ektoderm”), do nevertheless continue to accept without question Spee’s version of the mor- phological characters of his early implantation stages. That interpretation carried with it for Graf Spee—as it was logically bound to do—the total repudiation of the existence of any wall or layer of “‘hinfalliges Ektoderm.” The fundamental incompatibility of the two views of the constitution of the blastocyst will reappear in the further course of the argument of this paper.
Graf Spee’s denial of the existence of even an evanescent outer tropho- blastic layer in the implanted blastocyst has recently obtained energetic support from the findings of Dr Maclaren (loc. cit.).
It is the special object of the present communication to re-examine the grounds of the interpretation placed by Spee and Maclaren upon the consti- tution of the blastocyst of Cavia before, during, and immediately after im- plantation. .
I hope to be able to show reason for the belief that that interpretation is in some material respects erroneous and retrograde and that Selenka and Duval were after all not mistaken in their recognition, in early implantation stages, of an ectodermal outer wall of the blastocyst, albeit of a somewhat exiguous and transient character.
Spee’s analysis of the constitution of the Guinea-pig ovum prior to im- plantation is on the following lines: He refers to it as a blastocyst (“‘ Keimblase’’). Its cellular wall (‘‘Keimhaut’’) is said to consist, in the equatorial region, of a single layer of flattened cells. Over that polar area characterised as “‘ Implan- tationspol” (also as “‘Gegenpol”’), it is likewise a single layer, but the cells are more cubical. Over the other polar area, facing the uterine lumen and desig- nated ‘“Placentalpol,” he describes the cellular wall as showing a clump of cells (‘‘Zellballen”’) projecting into the cavity. Clearly the ovum thus de- scribed corresponds exactly to the typical early blastocyst of other Eutheria, though the author omits any attempt at comparison with other types.
In other passages Spee refers to the blastocyst wall or ‘“‘Keimhaut” indifferently as “aussere Zellhaut” and “aussere Eihaut.” On p. 189 he affirms of the implantation pole of the ‘‘aussere Zellhaut” that it “bildet nach der Implantation die freie Eikuppe, in die die Embryonalkugel spater hineinriickt und in der der Embryo sich ausbildet.”’
Now from an examination of his figs. 19 PA and 22 (cf. Plate I, fig. 8), it is perfectly evident that this “‘Kikuppe”—supposed by him to be identical with the implantation pole area of the early blastocyst—is none other than the cell layer which in its immediately subsequent history has obtained practically universal recognition as the “inverted” entoderm layer of the embryo.
It is true that I cannot find that Graf Spee himself does anywhere affirm or admit this identity but it is an inevitable consequence of the value he assigns to the layers of the implanted ovum of Cavia.
His position therefore involves the rejection—so far as the Guinea-pig is concerned—of that explanation of “inversion of the germ layers” which was furnished by Selenka. And it is to be associated, of course, with Spee’s em- phatic denial, already quoted, of the existence of a trophoblastic outer layer (‘‘Deckzellenschicht”’) in any way corresponding to that described and figured by Selenka and Duval in the Rat and Mouse and by Selenka in the Guinea- pig also.
Maclaren has arrived at similar conclusions, on this matter, to those of Graf Spee and he has not hesitated to make explicit the opinion, which we have seen to be implied in the statements of the latter author, that the definitive ‘in- verted”’ yolk-sac entoderm is actually the same cell layer as that which con- stitutes the so-called ‘‘implantation pole” area of the wall of the unimplanted blastocyst.
Both of these observers recognise and figure a blastocyst cavity as existing prior to implantation. Both of them hold that this cavity subsequently dis- appears during the process of implantation, either by collapse or by obliteration of the original cavity through increase of the “Zellballen” (inner cell mass) which is continuous with the “placental pole” of the early blastocyst. Thus for both of them the “ovum” during implantation is a solid morula with a central cellular core surrounded by an outer layer of cells. But whilst it would seem that Spee continues to regard the entire outer layer, including the “implantation pole” area or “Gegenpol” (his “Eikuppe”), as ectodermal, Maclaren, on the other hand, regards the latter area of the outer layer as certainly entodermal on account of its further destiny.
Now even apart from any question of homology, a reversion from the already attained condition of a normal Eutherian blastocyst to that of a solid morula would be an extraordinary phenomenon to manifest itself in the growing and developing ovum. It would be a retrograde change unparalleled in any other known Eutherian group, not excepting the closely related types of Rodents exhibiting “inversion” or “entypy.” In the latter the blastocyst on implantation not only retains its cystic cavity but for a time this increases in extent, subject only to the compression and modification in form occasioned by the further intrusion into it of the amnio-embryonic primordium with its ectoplacental suspensorium. Only later does the cavity lose its character as its outer wall becomes more or less vestigial.
Is it really credible, then, that the ovum of the Guinea-pig should differ so fundamentally from even its nearest congeners?
The excellent figures of the pre-implantation blastocyst of Cavia which both Spee and Maclaren supply (Plate I, figs. 1 and 2) indicate the possession of a structural constitution which is indistinguishable in all its essentials from that of other Eutheria of corresponding stages. Indeed it is clear that, apart from the question of the prospective significance of the various regions, no doubt could arise as to its identity with the latter. It exhibits a characteristic unilaminar “trophoblastic” wall with an inner “formative” cell mass (‘“‘em- bryoblast” of Rabl and Grosser) attached at one area of its interior.
Furthermore, the fact must not be ignored that Selenka (loc. cit.) has actually figured and described a series of successive stages of the blastocyst of Cavia in which he depicts in the most definite fashion the persistence, after implantation, of an outer trophoblastic wall, though in an obviously atrophying condition (Plate I, figs. 3-7).
In view of these positive records of Selenka I am unable to understand the statement of Maclaren (loc. cit. p. 117) that the presence of such a layer “has never been actually observed.” It may be admitted that Selenka’s figures are rather diagrammatic and I am ready to believe that he may have allowed him- self some latitude in the direction of restoration or reconstruction. In them- selves, therefore, they may not be admissible as conclusive evidence in regard to a disputed point. It should be remembered, however, that at that time the point was not in dispute and one is therefore entitled to regard his presentation of the case as at least more or less unbiassed. In any case, I find it hard to believe that what Selenka so very definitely delineates as an outer blastocyst wall in process of atrophic disappearance, in quite a number of different speci- mens (cf. Plate I, figs. 3-7), was wholly fanciful and merely the product of a vivid imagination.
I have myself made a careful study of serial sections of a number of early implanted blastocysts of Cavia, in situ in the uterine wall, from the Heape embryological collection in Cambridge.
Several of these are almost identical in stage with those illustrated in Spee’s figs. 19 PA and 22 (Plate I, fig. 8), in which the ectoplacental sus- pensorium has begun to take form as a discoid thickening.
In these I have been able to recognise delicate cellular alar extensions from the marginal region of the ectoplacental disc. These alae taper off into single cells. They correspond to the “Seitenfalten” of Spee’s fig. 22 (Pl. I, fig. 8) but they are very inappropriately described as folds. I am of opinion that Spee’s explanation of their character is erroneous and I venture to suggest that they are actually vestiges of the proximal attachment of the evanescent trophoblastic outer layer, the “‘hinfalliges Ektoderm,”’ auct.
In one of these specimens of Heape’s I am confident of the persistence of definite remains of the parietal trophoblast layer itself.
However that may be, I submit that in view (a) of the comparative rarity of material for the study of critical stages; (b) of the technical difficulties in avoiding disturbance of delicate structural relations; and (c) the probability of considerable individual variation in the condition of a layer in course of absorptive disappearance; it will not do summarily to dismiss the evidence offered by Selenka as wholly unworthy of serious consideration.
I propose now to enquire more closely into the source of the discrepancy between the accounts given respectively by Graf Spee and by Selenka. And I shall first claim as common ground—for reasons already given and in spite of Maclaren’s opinion to the contrary—the admission of a complete homology between the different regions of the unimplanted blastocyst of Cavia and the very similar regions of the early blastocyst of other Eutheria.
In this connection I reproduce for comparison (Plate IL, fig. 9) Duval’s illustration of the early (unimplanted) blastocyst of the Mouse. Here the essential correspondence with Spee’s and Maclaren’s figures (Plate I, figs. 1 and 2) from Cavia is unmistakable, the only obvious difference being that in the case of the Mouse the differentiation of a definitive entoderm layer from the deep surface of the inner cell mass, or “‘embryoblast,” has already taken place.
Plate II, fig. 10 shows a reproduction of Graf Spee’s important fig. 7. In it the author illustrates one of the initial phases of implantation in the Guinea-pig. It is one of Spee’s figures most commonly reproduced in text- books to illustrate the first step in “interstitial” implantation.
There is little difficulty in interpreting the condition of the ovum illustrated in this figure in terms of the normal Eutherian blastocyst, nor does the author himself introduce any discordant idea in his explanation of it. He still re- cognises the specimen as a “‘Keimblase” with a cystic cavity enclosed by the “Keimhaut” whose thin-walled implantation pole area has now become em- bedded, whilst the placental pole still protrudes into the uterine lumen.
It is in his reading of the structural features of his next succeeding stage (stage II) of the implanted blastocyst that Spee reveals his marked divergence from the views of previous observers.
The structural picture representative of the stage in question is shown by the author in several figures, one of which is here reproduced as Plate II, fig. 11.
It is deserving of notice that this stage was represented in Spee’s series by one specimen only; and, further, that of this sole specimen only one thick section, containing three or four superimposed nuclear layers, remained intact and available for exact investigation.
It must be admitted that the figures he gives of this section yield only a rather confused picture of its intimate structure. The author himself admits some difficulty in deriving its structural arrangements from the condition of the previous stage (“‘Wenn sich nun auch wegen der erheblichen Dicke des vom Ei vorliegenden Durchschnitts und der nicht besonders scharfen histo- logischen Differenzirungen der Gewebstheile durch die dazu angewandte Pikrinschwefelsiure pracisere Angaben den obigen sich nicht zufiigen lassen,” etc.). Nevertheless he considers himself justified in drawing the fairly con- fident conclusion that the single layer of cells which at one side clothes the larger cell mass (Plate II, fig. 11) represents the earlier “Keimhaut mit Gegenpol’”’; whilst the cell mass itself represents the “‘Keimhiigelregion” which has protruded into the former cavity of the blastocyst so as to gain contact with the “‘Gegenpol,” thus completely filling up the cavity.
Incidentally Spee notes the fact that the total calibre of the ovum has not only not increased but even shows a trifling diminution as compared with the immediately previous stage. Elsewhere he remarks concerning this pheno- menon “‘dass der Raum zwischen dem Zellballen und der hautahnlich diinnen ins Uterusgewebe vorgeschobenen Zelllage des Kies entweder durch Wachsthum des Zellballens ausgefiillt worden oder dass der Raum durch Collaps seiner Wand verschwunden sei.”
I venture here to suggest that even of the unsatisfactory and inconclusive picture offered by Spee’s figs. 8 and 8 P (cf. Plate II, fig. 11) an alternative explanation may be given. This is, that the original cavity of the blastocyst has not wholly disappeared but is still represented by the cleft-like spaces shown between the mass of cells and the supposed decidual zone surrounding it. Further, I suggest that the characters of the latter zone are attributable, not merely to a decidual reaction to the implanted ovum, but in part, at least, to the incorporation in it of material of the original trophoblastic ‘‘Gegenpol”’ of earlier stages. I suggest, indeed, that such an incorporation of atrophic trophoblastic material is already taking place even in the preceding stage shown in Plate II, fig. 10.
The next succeeding stages (III and IV) of Spee’s series are separated only by the briefest intervals of time from his stage II, and from one another.
In Plate II, figs. 12 and 18 are reproduced two of his illustrations of his stage III, whilst in Plate II, fig. 14 there is shown a reproduction of his well- known fig. 11 representing his stage IV. The latter figure has found its way into most of the modern text-books and has there been accepted at its author’s own valuation.
In all of these figures the apparent outer cell layer of the supposedly morular ovum now appears more definite and distinct. Where it covers the superficial surface of the mass and is still exposed to the uterine lumen it represents the ‘“‘placental pole” and its significance as ectoplacental tropho- blast is obvious and unquestionable. Its cells are specifically referred to by Spee (loc. cit. p. 174) as becoming the mother cells of the foetal placental tissue.
The question therefore arises: Is the remainder of this apparently con- tinuous outer layer, where it covers the deep surface of the inner cell mass, to be regarded as of the same ectodermal (trophoblastic) nature as the superficial, placental pole, area with which it appears to be directly continuous? According to Spee, it is constituted by the original implantation polar area (‘‘Gegenpol’’) of the ‘‘Keimhaut” or “‘aussere Kihaut.” If so, its homology must certainly be with the thin trophoblastic wall of the ordinary Eutherian blastocyst.
On the other hand, there can be no doubt that, as Maclaren quite rightly insists, this same layer, which at this stage clothes the deep surface of the morula-like mass, is genetically identical with the layer of ‘‘inverted”’ ento- derm of later stages. Maclaren nevertheless follows Graf Spee in identifying it with the thin implantation pole area of the wall of the unimplanted blastocyst.
In this latter identification I am convinced that both Spee and Maclaren are in error. The very definite layer covering the deep surface of the inner cell mass in Spee’s stages III and IV, as well as later, has, I suggest, nothing to do with the thin wall of the early blastocyst but has itself been delaminated or differentiated as entoderm from the deep surface of the early inner cell mass itself. Its apparent continuity with the admittedly trophoblastic superficial covering of the inner cell mass is merely topographical and secondary, not genetic and primary. (Incidentally it may be noted that a comparison of Spee’s figures suggests that the central core of cells of the inner cell mass appears to have undergone reduction during this suggested process of differen- tiation from it of an entodermal layer. But it would be rash to attach too much importance to this distinction.) I further suggest that on the evidence furnished by various illustrations of the structure of the unimplanted blasto- cyst of Cavia (Plate I, figs. 1 and 2) the question may well be raised whether the process of differentiation of entoderm may not already have begun prior to implantation, as appears to be the case in the Mouse (Plate II, fig. 9).
On the other hand, if Spee’s interpretation of his stages III and IV be correct, it is well to recognise clearly what its acceptance implies. In the first place we shall have to recognise the occurrence of the extraordinary phe- nomenon of a sudden and complete obliteration of the already existing blastocyst cavity in a growing and developing ovum, i.e. its sudden reversion to the condition of a typical morula. In the second place we have to witness the strange and rapid transformation of the atrophic and exiguous distal wall of the blastocyst of Spee’s fig. 7 (cf. Plate II, fig. 10) into a closely fitting layer of active, well-formed, cells which can easily be followed through. all subse- quent stages into the conspicuous columnar layer ensheathing the embryonic rudiment and as such universally recognised as inverted entoderm!
In opposition to this view I submit with some confidence the opinion that the phenomena exhibited by the blastocyst of Cavia during implantation are susceptible of an explanation less at variance with our knowledge of the characters of the early blastocyst in other “‘entypical” Rodents.
In order to bring out more clearly what I believe to be the true reading of Spee’s and Maclaren’s figures of the blastocyst of Cavia I reproduce herewith four figures of stages in the development of Arvicola, another member of the group of Rodents showing “inversion,” as illustrated by Dr Sansom (10) in 1922.
The first of these (Plate III, fig. 15) may profitably be compared with Spee’s figure of a very early blastocyst of Cavia (Plate I, fig. 1). In this latter figure I have suggested above that there is already some indication of commencing differentiation of the primordium of the entoderm from the “embryoblast” or formative inner cell mass, though I attach no great import- ance to this point. The Arvicola figure shows a somewhat flattened blastocyst towards the beginning of implantation. Here, at the so-called “placental pole” of Spee, we have a discoidal plate-like area of cubical trophoblast cells to whose deep surface the inner cell mass is attached. The character of this trophoblast disc already foreshadows the ectoplacental suspensorium or “Trager.” This is continuous marginally with the thin non-placental tropho- blastic wall of the blastocyst which distally corresponds to the “implantation pole” area of Spee. As in the Guinea-pig, the cystic cavity is not very ex- tensive and within it two small cell groups very probably represent entoderm beginning to be differentiated from the embryoblastic inner cell mass.
This structural conception is entirely borne out by the features of the next stage as seen in Plate III, fig. 16. On a merely casual glance at this figure one might be led to identify the now definite layer of entoderm with the thin trophoblast wall of the previous figure. To do so would be precisely to repeat what I believe to be the radical mistake of Graf Spee in the case of Cavia. A more attentive study of the figure will make it perfectly clear that the former trophoblast wall is still present although it now takes the form of a more or less syncytial layer closely applied to, and even partly incorporated with, the surrounding decidual zone.
The next succeeding stage in Arvicola (Plate IV, fig. 17) shows the ento- dermal layer now in the form of a completed vesicle, a condition which it never attains in the Guinea-pig. But the distal trophoblast wall—whilst preserving its marginal continuity with the ectoplacental disc—still persists as a some- what mutilated, but nevertheless more or less continuous layer. And here I would direct special attention to the very definite preservation, in somewhat cuticular form, of the inner boundary of this now rather imperfect and more or less syncytial layer.
In a still later stage of Arvicola (Plate IV, fig. 18) the distal wall of the entodermal vesicle has now largely disappeared. Also the distal trophoblast wall has undergone further atrophy, probably ‘through cytolytic change, almost to the point of disappearance. It is now little more than a thin syncytial or perhaps symplasmatic lining to the decidual encapsulating tissue. Nevertheless its inner cuticular-like boundary is still preserved, thus definitely limiting the original blastocyst cavity, whilst the original marginal connection with the now thickened ectoplacental disc is still maintained.
In the light of these illustrations of the constitution of the developing blastocyst of another “entypical” Rodent we may now return to the considera- tion of the condition in the Guinea-pig as seen in Graf Spee’s series of figures. It is unnecessary to recapitulate the critical analysis of the figures already commented upon in previous pages. The alternative explanation of them already suggested is, I submit, elucidated and confirmed by the appearances presented by Arvicola.
Spee’s celebrated fig. 11, however (Plate II, fig. 14), perhaps deserves some further remark on account of its general acceptance and reproduction in various treatises as exemplifying the alleged solid morular condition of the embedded ovum of Cavia. Thus in his recent work Grosser ((6), 1927) definitely accepts the morula-concept in the following terms: “Eine wohlausgebildete, vielzellige Morula, wie wir sie beim Kaninchen oder den Fledermausen finden, laszt nun (als weitere Verschiedenheit gegeniiber niederen Vertebraten) einen deutlichen Unterschied zwischen einer oberflachlichen einreihigen Zellschicht und dem inneren Zellhaufen erkennen; die beiden Anteile entsprechen, wie die weitere Entwicklung lehrt, einerseits der Anlage des Chorionektoderms, anderseits der Anlage aller tibrigen Teile, also vorziiglich des ganzen Embryos,” ete.
On the other hand, Grosser does. not follow Spee in entirely rejecting the idea of the temporary existence of a layer of “‘hinfalliges Ektoderm.” In regard to this he would appear to follow the lead of Selenka and Duval; but he does not appear to have made any attempt to harmonise this view with the morula view of Spee. He does not betray any consciousness of their mutual incompatibility.
Accordingly he must be understood to believe (a) in agreement with Spee, that there is in the unimplanted blastocyst a thin trophoblastic wall; (b) also in agreement with Spee, that this wall becomes, on implantation, the outer layer of a solid morula; (c) in opposition to Spee, that somehow or other a thin and evanescent trophoblastic layer (“‘hinfalliges Ektoderm”’) comes to form the outer wall of the developing blastocyst. It is true, however, that although Grosser has not realised the incompatibility between the two views he espouses he is not completely satisfied with the position as it stands. This is evident from his remark ((6), 1909, p. 71), in reference to the constitution of the supposed implanted morula of Spee, “doch ist das Schicksal dieser Abschnitte noch nicht hinreichend verfolgt.” Notwithstanding this he still, in 1927, accepts, in common with such other well-known authorities as Hertwig (loc. cit.), Bonnet (11) and Corning (12), the morula-like embryonic structure so prominent in Plate II, fig. 14 at the value attributed to it by Graf Spee. I again submit that the true reading of this figure is in terms of the process so clearly manifest in the series of figures of Arvicola.
When this figure is compared with Plate III, fig. 16, which repeats Sansom’s text-fig. 2, the fundamental similarity of the two conditions is at once ap- parent. The only outstanding difference between them is that in Arvicola the antembryonic trophoblastic wall of the blastocyst has not yet wholly lost its identity—as later on it will—in the decidual surroundings.
In Plate V, fig. 19 is reproduced another of Spee’s figures of a specimen which he classifies as belonging to the same stage IV. Although the author remarks that the figure does not afford an accurate understanding of the structural condition it is, in my opinion, deserving of attention. It appears to me that it falls perfectly in line with his important fig. 7 (Plate II, fig. 10) as exhibiting a slightly later phase. The conspicuous vacuolated spaces in Plate V, fig. 19 actually occupy the same relative position as the admitted blastocyst cavity in Plate IT, fig. 10. The author however explains them quite differently—as liquefaction cavities in the midst: of a symplasma resulting from histolytic change in the surrounding decidual tissue. On the lines of the process seen in Arvicola and indicated in Spee’s own fig. 7 (Plate II, fig. 10, mihi) I suggest that the supposed liquefaction cavities really represent the original small blastocyst cavity crossed by strands of coagulum. I further suggest that in the peripheral zone, marked “1” in the figure, there is to be recognised the site, and probably in part the vestiges, of the original thin ‘implantation pole” area of the blastocyst. I consider it beyond doubt that the cell layer now clothing the deep surface of the embryoblastic cell mass is entodermal in character and never at any time formed part of the original blastocyst wall.
In Plates V, VI, figs. 20-23 I herewith reproduce four other figures from Graf Spee’s paper (his figs. 12 P’, 13 4,17 A and 15). All of these figures show more or less similar features. All of them show the same morula-like mass, clad on its deep surface by a single layer of cells which is indubitably the future ‘‘inverted”” entodermal layer. All of them show the solid cell mass as partly sur- rounded by a more or less crescentic clear space, Spee’s “‘Saftraum”; Maclaren’s ‘destruction space.” All of them show this space to be limited peripherally by a sharp cuticular-like boundary—a condition very unlikely to result from a process of cytolytic destruction, where an irregular or. ragged boundary would be much more likely. The decidual zone thus sharply limited irresistibly suggests the same explanation as the corresponding zone in Arvicola, of a syncytial or perhaps rather a symplasmatic compound of trophoblastic and decidual elements. In short, all the features exhibited by these figures of Graf Spee may best be explained on the lines laid down in the preceding pages.
The general conformity of Maclaren’s figures of similar stages is unmis- takable as will be evident from a comparison with Plate VI, figs. 24-5, which reproduce his figs. 2 and 8.
It is noteworthy that at the definitely later period corresponding to that of Spee’s figs. 18-22 (Plate I, fig. 8); to Maclaren’s fig. 5 and to similar specimens in the Heape collection; the cuticular boundary of the quondam blastocyst cavity breaks down more or less completely. But in the critical stages now specially under consideration the definite sharp boundary seems to be constant and the identity of the picture during this phase with Plate IV, fig. 18, after Sansom, is most striking.
Thus far no detailed reference has been made to the comparatively recent work of Pytler and Strasser(8) which deals with the development of Cavia subsequent to implantation. But inasmuch as the earliest stage personally investigated by these observers was one in which the amnio-embryonic primordial mass was already widely separated from the ectoplacental sus- pensorium their observations throw no light on the problem under discussion.
It may be noted, however, that in their résumé of the facts of earlier development they appear to follow Graf Spee closely in reference to the phe- nomena of implantation (apart from a probably inadvertent misapplication of Spee’s term ‘‘Gegenpol’’). In their conception of what may be called the post-implantation stage, on the other hand, they appear, like Grosser, to follow Duval. Their schematic figures, reproduced by Grosser in his latest work (loc. cit. 1927), are obviously founded on Duval’s. They have not made any attempt to determine how the post-implantation vesicular blastocyst of the Duval scheme is derived from the solid “morula” of Graf Spee.
In view of the foregoing critical review of the evidence furnished by Spee and Maclaren I suggest, with all respect to these observers, but with some degree of confidence, that the structural features of the early implanted blasto- cyst of Cavia ought to be interpreted not in the sense of their presentment, but rather along the lines which I have illustrated by means of Dr Sansom’s figures of Arvicola.
It is evident that this interpretation will bring the process of development in the Guinea-pig once more into harmony with that of the other Rodents which exhibit the phenomena of “entypy” in their early development. In other words I contend that the morphological interpretation of the blastocyst of Cavia which was entertained by Selenka and Duval is fundamentally valid and correct and that Spee’s later contribution—apart from the value it may still possess from the point of view of the method of implantation—has had the unfortunate result of introducing an unnecessary confusion into the current conception of the morphology of the blastocyst in this Rodent type.
In conclusion, I desire to reiterate that I make no claim in this paper to contribute new and original observations of the phenomena under considera- tion. My aim has been simply that of critical discussion and reinterpretation of facts and observations which are already on record in word and figure.
I am indebted to the Royal Society of Edinburgh for permission to reproduce figs. 2, 24 and 25 from Dr Maclean’s paper on ‘“‘ Development of Cavia: Implantation,” appearing in their Transactions, vol. Lx, pt 1, to the publishers of the Zeitschrift fiir Morphologie und Anthropologie for figs. 1, 8, 10-14 and 19-28, to C. W. Kreidel’s Verlag for figs. 8-7, and to Librairie Félix Alcan for fig. 9 from Duval’s Le Placenta des Rongeurs.
(1) MacraRreEn, N. (1926). Trans. Roy. Soc. Edin. vol. tv, p. 115. (2) Biscnorr, Tu. (1852). Entwicklungsgesch. d. Meerschweinchens. Giessen. (3) SzLenKa, E. (1882, 1883-5). Studien iber Entwicklungsgesch. 1 and 111. Wiesbaden. (4) Duvat, M. (1889). Journ. de [ Anat. et de la Physiol. (1889-92). Republished, Paris 1892. (5) Herrwie, O. (1906). Handbuch d. vergl. u. exper. Entwicklungslehre. Bd. 1, pp. 915 ff. (6) Grosser, O. (1909). Hthdute u. d. Placenta. Wien and Leipzig. . —— (1927). Frithentwicklung, Eihautbildung u. Placentati Miinchen: Bergmann, 1927. (7) Fraser (1882). Nature, vol. xxvi, p. 493 (Sept. 14, 1882). (8) Pytuer, R. and Strasser, H. (1925). Zeitschr. f. Anat. u. Entwicklungsgesch. Bd. Lxxvt. (9) Sprx, F. Grar (1901). Zettschr. f. Morph. u. Anthrop. Bd. m, p. 130. (10) Sansom, G. 8. (1922). Journ. of Anat. vol. Lv1, p. 333. (11) Bonnet, R. (1920). Entwicklungsgeschichte, fig. 158. (12) Cornine, H. K. (1925). Lehrbuch d. Entwicklungsgesch. fig. 106.
Explanation of Plates
Fig. 1. Spee’s fig. 6, blastocyst of Cavia of 6 days, 11 hours, with still intact zona pellucida and free in uterine cavity near a shallow epithelial fossa. It shows the typical characters of an early Eutherian blastocyst with unilaminar trophoblast wall and inner cell mass or “embryoblast”’ attached at one pole. It seems probable that the differentiation of the entoderm from the deep surface of the embryoblast has already begun.
Fig. 2. Maclaren’s fig. 1, showing blastocyst of Cavia exhibiting essentially similar characters to those of fig. 1. Maclaren gives the age as 5 days. The blastocyst lies in a fossa or crypt of the uterine mucosa whose epithelium is yet intact.
Figs. 3-7. Reproductions of Selenka’s figs. 3-7, representing blastocysts of the period from 6 to 7 days. In each of these a thin trophoblastic wall is figured, although it is relatively incon- spicuous and in most cases evidently atrophic. In all except fig. 3 the separation between the embryoblast and the ectoplacental disc or “Trager” has already begun, whilst in fig. 6 the ectoplacental cavity is also indicated. The proximal or “visceral” layer of entoderm, clothing the deep surface of the embryoblast, is clearly differentiated. It has at these stages the ap- pearance of being continuous with the ectoplacental trophoblastic disc. Genetically, however, it is certainly derived from the embryoblast which it covers (cf. fig. 9 of early stage of Mouse).
Fig. 8. Spee’s photographic fig. 22, representing an implanted blastocyst of Cavia of 7 days. Here it is evident that the separation of the embryoblastic from the ectoplacental primordia is beginning. In accordance with his general view Spee regards the unicellular layer clothing the projecting embryonic mass as “aussere Eihaut””—the original implantation pole area of the blastocyst wall. According to the view enunciated in the present communication it is clearly entoderm. For further discussion of this figure see text, p. 356.
Fig. 9. Duval’s fig. 79, early blastocyst of Mouse (two sections); the resemblance to the early blastocyst of Cavia (figs. 4 and 2) is obvious, though the differentiation of entoderm from the embryoblastic inner cell mass is here quite determinate.
Fig. 10. Spee’s fig. 7, blastocyst of Cavia of 6 days, 10 hours, showing early phase of implantation process. The zona has disappeared. The inner cell mass is relatively large. The trophoblastic outer layer marked a is seen to extend deeply into, and around the periphery of the im- plantation fovea. The two small vacuoles shown at v lie in cytoplasmic material representing the original trophoblast wall. Spee himself refers to it as “‘das haiutige Theil des Kies.” The clear spaces e he regards (with justice) as the cavity of the ovum.
Fig. 11. Spee’s fig. 8, representing his implantation-stage II. See discussion in text, pp. 351-2. 12. Spee’s fig. 9 B, representing his implantation-stage III. According to the author this figure illustrates the obliteration of the blastocyst cavity which was still present in the speci- men shown in fig. 10 (supra). For him, the layer of cells now seen enclosing the central cell mass is the same layer which in fig. 10 lines the implantation fovea. The contention of the present paper is that the latter layer—already more or less atrophic in fig. 10—has now practically disappeared by incorporation in the decidual zone and that the well-marked layer covering the central mass on its deep aspect is the now well-differentiated entoderm.
Figs. 13-14. Spee’s figs. 10 and 11; the author takes fig. 14 as the type of his implantation- stage IV, fig. 13 as belonging to the preceding stage. In all essentials they are, however, very similar. Fig. 14 has been frequently copied by other writers as illustrating the assumed morula stage of the implanted ovum of the Guinea-pig. The suggestion of the present paper is that the crescentic clear cavity surrounding the morula-like mass (Spee’s “‘Saftraum”) is in reality the representative of the original cavity of the blastocyst whose outer trophoblastic wall is still represented by vestigial material incorporated in the obviously much modified decidual zone around it. The cell layer clothing the central mass of cells towards the cavity is the entoderm.
Figs. 15-18, Sansom’s text-figs. 1-4, illustrating the blastocyst of Arvicola amphibius during early stages of implantation. This series of figures is held to furnish the key to the correct inter- pretation of the constitution of the early implanted blastocyst of Cavia. In these figures the fate of the original trophoblast wall may be followed, up to the period of its merging, as a vestigial layer, with the decidual capsule. The entodermal relationships are worthy of special attention in their bearings upon the problem of the entoderm in Cavia.
Fig. 19. Spee’s fig. 16, to be specially compared with fig. 10. See p. 355 of the text.
Figs. 20-23. Spee’s figs. 12 P’, 13 4, 17 A and 15; the characteristics of these four figures are essentially similar. See p. 356 of text.
Figs. 24-25. Maclaren’s figs. 2 and 3; these figures are obviously open to the same analysis, and demand the same explanation, as figs. 20-23. See p. 356 of text.
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