The Eggs of Mammals (1936) 4

From Embryology

Chapter IV The Development and Atresia of the Fully Grown Ova and the Problem of Ovarian Parthenogenesis

The Eggs of Mammals (1936): Introduction | The Origin of the Definitive Ova | The Growth of the Ovum | The Development and Atresia of Full-Grown Ova and the Problem of Ovarian Parthenogenesis | Methods Employed in the Experimental Manipulation of Mammalian Ova | The Tubal History of Unfertilized Eggs | Fertilization and Cleavage | The Activation of Unfertilized Eggs | The Growth and Implantation of the Blastodermic Vesicle | Summary and Recapitulation | Bibliography | Figures | Historic Disclaimer
Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Even when the ova have attained maximum size a majority of them are destined to degenerate. We have already mentioned that Allen, Kountz and Francis (1925) estimated that only 14 per cent of the medium sized follicles of the pig ovary attain maturity. Engle (19276) finds that in the mouse the percentage of atresia among follicles with antra varies with the stage of the oestrus cycle, the maximum percentage of 86 per cent being recorded at the cornified cell stage. While the percentage of atretic follicles with mature ova was highest at the oestrus stage the maximum number was observed at the beginning of the dioestrus. This is obvious from the data of Table V and Figure 13 which summarize the data on 50 ovaries from nonpregnant mice taken at four stages of the cycle. These data include small atretic follicles as well as antrum-containing folUcles, but the fact that the data for pseudomaturation spindles (which occur only in full sized ova) parallel those for follicles indicates that the total number of atretic mature ova reach their maximum in early dioestrus shortly after ovulation. This is doubtless due to the continued formation of antrum-containing foUicles at a fairly high rate for a short time after ovulation.

We have seen that ovogenesis continues during pregnancy. Engle's data demonstrate that the formation of ova also occurs during pregnancy, for he observed an t.§ appreciable number of c^gio pseudomaturation spindles in ovaries taken during the first 43/2 days of pregnancy. These data are summarized in Table VI and Figure 14. It is notable that both the total amount of atresia and the atresia of mature ova is less throughout this period spindles in the median ovary at four than during the period of stages in early pregnancy in the mouse. 1 i J i J- • (From the American Journal of Anat least destruction m non- ^^^^y^ pregnant mice. Unfortunately, Engle does not give the percentages of atresia during early pregnancy.


Fig. 13. Showing the number of atretic folUcles and pseudomaturation spindles in the median ovary at four stages of the oestrus cycle in the mouse. (From the American Journal of Anatomy.)


TABLE V

The Degree of Atresia of Ovarian Follicles of the Mouse at Four Stages of the Oestrus Cycle. (From Engle, 1927b)


Stage

OF

Cycle

Median

OF

Spindles

Average

OF

Spindles

Range

OF

Atresia

Median OF Total Atresia

Average OF Total Atresia

Range of Total Atresia

Corn

16

18.5

6-40

59

60

36- 85

LEI

26

28.4

7-51

71

77.9

50-129

LE2

11

11.2

5-17

36

42.1

29- 63



13

12

0-26

39

39.8

15- 70



30


and atresia of full-grown



ova also occurs during pregnancy, for he observed an t.§ appreciable number of c^gio pseudomaturation spindles in ovaries taken during the first 43/2 days of pregnancy. These data are summarized in Table VI and Figure 14. It is notable that both the total amount of atresia and the atresia of mature ova is less throughout this period spindles in the median ovary at four than during the period of stages in early pregnancy in the mouse. 1 i J i J- • (From the American Journal of Anat least destruction m non- ^^^^y^ pregnant mice. Unfortunately, Engle does not give the percentages of atresia during early pregnancy.



Fig. 14. Showing the number of , , , i ii • • 1 atretic follicles and pseudomaturation


The presence of cycles of atresia and growth in animals other than the mouse has already been noted (Evans and Swezy, 1931). According to Asami (1920) the rabbit exhibits a constant rate of follicular atresia before and after pregnancy. Pincus and Enzmann (19366) found that the younger folUcles (types 1, 2 and 3 — Plate III) of the rabbit show a much lower percentage of atresia than the larger follicles.

TABLE VI

The Degree of Atresia of Ovarian Follicles of the Mouse Stages of Early Pregnancy. (From Engle, 19276)

AT Four

Stage of Tubal Ova

Median

OF

Spindles

Average

OF

Spindles

Range

OF

Spindles

Median OF Total Number Atresia

Average OF Total Number Atresia

Range of

Total

Number

Atresia

To 2 pronuclei 2 to 4 blastomeres Morula Blastocyst

5 2 3

6

5

2.5 5.6 7.1

0-15 0- 7 2-20 3-14

22

17 13 15

23 18 16.5 17.3

11-41 10-31

7-38 14-28


The atresia of mature ova can be prevented by pituitary hormones. This is deduced from the phenomenon of superovulation observed in animals receiving pituitary implants (Smith and Engle, 1927; Smith, 1932). These authors describe, for example, the presence of 49 ova in the tubes of a mature mouse receiving anterior lobe implantations. An adult mouse produces from six to twelve corpora lutea at an ovulation, the absolute number varying with weight of the mouse, the number of previous pregnancies, and certain genetic factors (MacDowell and Lord, 1925; MacDowell, Allen and MacDowell, 1929). In Smith and Engle's mice the largest number of ova ever found in one tube of a normal mouse was seven, and in an immature mouse showing superovulation a maximum of 48 ova was observed in a single tube. Thus the maximum number normally found in one tube is 14.5 per cent of the maximum number super ovulated. Furthermore, if we assume from MacDowell's data that 9 is roughly the number of ova normally ovulated this is 18 per cent of the 49 superovulated in the adult mouse. These percentages agree with the estimations of per cent of antrum-containing follicles maturing. The paucity of antrum-containing follicles and reduction of atresia is directly noted by Smith and Engle. Finally, the ovulated ova are fertilizable although Engle (19316) found evidences of the degeneration of a number of them in the fallopian tubes.


An interpretation of the foregoing data is that normally only a limited amount of pituitary secretion is available to the ovary and consequently only a certain percentage of the ova are able to obtain the amount necessary to prevent their atresia, whereas in animals receiving large amounts of pituitary hormones from implants an abnormal number of ova have available sufficient amounts of atresia-suppressing hormones. It cannot be decided, however, whether the effect on the ova is directly exerted by these hormones, or whether the stimulated follicle tissue produces substances ensuring normal ova, or whether some extraovarian substance released into the circulation by pituitary stimulation reacts upon the ova.


Loeb (1917; see also Meyer, 1913) has indeed suggested that the ovum itself is the controlling factor in follicle development citing the frequent presence of mitoses in follicle cells adjacent to the ovum as well as certain histological evidence that the cumulus oophorus develops under the influence of the ovum (Walsh, 1917). Allen and his collaborators (1924) also maintained that the ovum is the dynamic center of the follicle apparently on the assumption that the mitosis-inducing action of oestrin upon vaginal and uterine epithelium is reflected in the higher mitosis rate in cells adjacent to the ovum becausB the ovum either produces oestrin or induces oestrin formation. In the opossum the presence of many atretic ova is correlated with prolongation of the dioestrus interval (Hartman). This supposed oestrinogenic action of the ovum has, however, been largely controverted (1) by the discovery of oestrin in corpora lutea as long as two weeks after ovulation (see Allen, 1932) and (2) by the observation that oestrin is produced in x-rayed ovaries lacking ova (Parkes, 1926-27). This evidence, however, does not prove that normally oestrin-production may not be under the control of the action of pituitary hormones upon the ovum itself.


In fact, aside from the presumable atresia-inhibiting influence, there seems to be only one other clearly evident influence of pituitary hormones upon the activities of the ovum. That is that the production of the first polar body is dependent upon stimulation by pituitary hormones.


Fig. 15. Ovum removed from a preovulatory follicle of an unmated rabbit showing the vesicular nucleus. (From the Journal of Experimental Medicine.)


Since this phenomenon is of some consequence to any discussion of the activation of mammalian eggs the writer, in collaboration with Dr. E. V. Enzmann (Pincus and Enzmann, 1935), has undertaken an examination of the mechanism of polar body formation in the rabbit ovary. The rabbit was chosen for these experiments because it ovulates only after copulation and the ova are liberated regularly between 93^ and 103^ hours after copulation (see Heape, 1905; Walton and Hammond, 1932; Pincus, 1930; Pincus and Enzmann, 1932). Furthermore, the mature ova form polar bodies only after copulation. According to Heape (1905)two polar bodies are formed in the ovary by 9 hours after copulation. Our observations indicate that only the first polar body is given off in the ovary and then the metaphase plate of the second polar spindle is formed. Robinson (1918) observed in the ferret, which also ovulates only after copulation, that only the first polar body is given off in the ovary some time after copulation.


Fig. 16. Ovum removed from a ripe follicle of a rabbit doe at two hours after copulation. Note beginning of chromatin condensation. (From the Journal of Experimental Medicine.)

Before copulation occurs the mature ovum contains a single large vesicular nucleus about 30 microns in diameter (Figure 15; see also Plate III, Figs. 4 and 5). At two hours after copulation signs of change are partially evident: some of the ripe ova show the beginnings of tetrad formation in the nucleus but the nuclear membrane is still intact (Figure 16). By four hours after copulation the tetrads of the first polar spindle are formed and the nuclear membrane is ordinarily dissolved (Figure 17). The metaphase plate has a diameter of a little over 10 microns. The first polar body is given off and the second polar spindle formed at or shortly after 8 hours post coitum (Figure 18). The follicle enlarges during this period also, the first signs of follicular development being evident at two hours after copulation. An exactly similar sequence of events occurs when prolan (pregnancy urine extract) or anterior pituitary extracts are injected.


Fig. 17. Ovum from follicle of ral)l)it don taken 4 hours after copulation. Formation of metaphase plate and dissolution of nuclear membrane. (From the Journal of Experimental Medicine.)


It has been definitely established that prolan and anterior pituitary hormones cause ovulation when injected into the rabbit (Bellerby, 1929; Friedman, 1929). The ovulation occurring after copulation occurs because of the increased level of pituitary hormones secreted into the blood. This level is increased by nervous stimulation of the pituitary consequent on the orgasm. It has been shown by Deansley, Fee and Parkes (1930) that hypophysectomy within one hour of copulation prevents ovulation in the rabbit (see also Smith and White, 1931), and McPhail fl933) has demonstrated similarly that the critical period of secretion increase in the ferret occurs during the first hour of coitus. It seems evident, therefore, that pituitary secretions are responsible for the activation of the egg resulting in the formation of the first polar body and the second polar spindle. Furthermore, certain observations of Hinsey and Markee (1933) indicate that the threshold for activation is lower than the threshold for ovulation. They observed that ovulation does not occur in large sized (2.6 kilograms and over) hypophysectomized rabbit does if prolan injection is made more than four hours after hypophysectomy. And in small sized hypophysectomized does (less than 2.3 kilograms) prolan ovulation never occurs. Nonetheless in all non-ovulating does polar body formation took place. Friedgood and Pincus (1935) found that stimulation of the cervical sympathetic of the rabbit resulted in maturation phenomena in those preovulatory follicles which failed to liberate ova. The sympathetic nerves presumably stimulated in these cases the secretion of sub-ovulatory amounts of hormone from the anterior pituitary. Finally, Pincus and Enzmann (1935) found definite ovum maturation with as little as 34 the minimal ovulating dose of maturity hormone.


Fig. 18. Ovarian ovum of rabbit doe mated 9 hours previously. First polar body and second polar spindle. (From the Journal of Experimental Medicine.)


In the ovaries of rabbit does which have copulated and then received pituitary injections within six hours after copulation the writer has observed the accelerated ripening of a new set of follicles and the formation of the first polar body. In these rabbits no accessory ovulation occurred though the pituitary extract dosages were at least two to three times greater than those necessary to cause ovulation in unmated does. The absence of ovulation indicates presumably that the expulsion of ova can occur only from full sized follicles, whereas the activation processes may be initiated in ova whenever a sufficiency of pituitary hormones are available. It should be neted, however, that the nuclear activity occurred only in medium sized follicles and never in follicles without antra or with small antra forming. Since the ovum in the rabbit grows to some extent after antrum formation (see Figure 11) it is possible that functional maturity is attained at some time after antrum formation. A new crop of follicles begins to mature in the mated rabbit, and may certainly be stimulated to ovulate by the 4th day of pregnancy as Wislocki and Snyder (1931) have demonstrated by producing superfetation at that time with simultaneous pituitary extract and sperm administration. It is evident, therefore, that any attempt to dissociate in vivo the processes involved in polar body formation and those involved in ovulation depends in the mature rabbit upon hormone administration during the very short interval of time following copulation in the hope that active substances reaching the medium sized follicles will differentially affect foUicular growth and ovum maturation.


Since the pituitary secretes a thyroid-stimulating as well as a gonadotropic hormone it is possible that maturation (and ovulation) is due directly to thyroid activity and only indirectly to pituitary stimulation. Pincus and Enzmann (1935) tested this possibility by injecting crystalline thyroxin and thyroprotein into rabbit does on heat. In no instance did ovulation occur but large doses of thyroxin did initiate follicular atresia and a limited degree of o\aim maturation. Again we see that atresia-inducing conditions also initiate maturation. The common feature of atretic follicles and preo\ailatory follicles is an isolation of the ovum from its connections with the follicular epithelium.


It is safe to conclude from the foregoing analysis that the formation of the first polar body in the rabbit ovary (and in the ferret's also) is dependent upon an increase of pituitary hormones in the circulating blood. It happens that in all spontaneously ovulating mammals except the dog the formation of the first polar body occurs in the ovary. Even in the dog (Evans and Cole, 1931) certain signs of nuclear maturation are observable in ovarian eggs. It is natural to infer that in spontaneously ovulating animals the pituitary level reached during oestrus is normally sufficient to induce ovulation as well as polar body formation.


Now it is notable that the atresia of ovarian eggs is often initiated by the formation of a maturation spindle. We have noted that Engle has designated the spindles of ova destined to atrophy as '^pseudomaturation" although there is no evidence that they are in fact typically unlike those observed in normally maturing ova. Such spindles are observed only in ova of full size. Measurements of spindle containing ova in mouse ovaries give an average maximum diameter of 70 microns, and mature ova with vesicular nuclei had an average of 69 microns. The writer has also made careful examination of a large number of rabbit ovaries and has never observed typical spindles in immature eggs. What ordinarily occurs is a complex fragmentation of the chromatin (see Figure 19). That the spindles are the indices of impending atresia is indicated by the observation that when they are at a maximum the total follicular atresia is also at a maximum (see Figures 13 and 14). A possible interpretation of their presence may be that they occur as a result of pituitary hormone action and the subsequent atresia of the ova containing them occurs because these ova are not Uberated and fertihzed. " Pseudomaturation " spindles have not been reported in hypophysectomized animals although atresia has.


Fig. 19. Atretic ovum from type 3 follicle in the rabbit. Note fragmentation of cytoplasm and chromatin.


It has long been the contention of certain observers of ovarian atresia that the apparent parthenogenetic development of ova destined never to be liberated is simply an incident of the process of degeneration and is not in fact true parthenogenesis (Hensen, 1869; Balfour, 1882; Sobotta, 1899; Janosik, 1897; Bonnet, 1899; Rubaschkin, 1906; Athias, 1909; Kingery, 1914; Kirkham, 1916; Stockard and Papanicolou, 1917; Addison, 1917; Long and Evans, 1922; Clark, 1923; Engle, 19276; Kampmeier, 1929). These investigators have observed varied types of fragmentation of egg nucleus and cytoplasm, most of which cannot be considered the result of true cleavage processes though in some instances a remarkable resemblance to cleaved ova is attained (see Plates IV and V). Another group of investigators generally admit that complex pseudoparthenogenetic fragmentation occurs, but claim that a varying number of ova enter into true parthenogenetic development (Pfluger, 1863; Flemming, 1885; Paladino, 1887; Lowenthal, 1888; Schottlander, 1891; Henneguy, 1893; Grusdew, 1896; Rabl, 1898; Gurwitsch, 1900; Spuler, 1900; Van der Stricht, 1901; Loeb, 1901, 1905, 1911, a and b, 1912, 1915, 1923, 1932; Newman, 1912, 1913; Sansom, 1920; Haggstrom, 1922; Courrier and Oberling, 1923; Courrier, 1923; Branca, 1925; Bosaeus, 1926; Lelievre, Peyron and Corsy, 1927). The resolution of such alternative points of view depends first of all upon a clear definition of what parthenogenesis is and secondly upon the interpretation of the ovarian structures designated as embryonic.


If by parthenogenesis is meant the development of a mature individual from an unfertilized egg then it is at once certain that parthenogenesis does not take place in mammalian ovaries. If, on the other hand, a cleavage of the ovum with an equational division of the chromosomes is the criterion then there is some evidence (Sansom, 1920; Branca, 1925; Engle, 19276) that occasionally parthenogenesis occurs in ovarian eggs (see Plates IV and V). Certainly it is not permissible to consider as parthenogenesis an exact reproduction of events taking place in the fertilized egg, since it is well known, for example, that parthenogenetic individuals arise from ova in which second polar body formation is suppressed.


It seems appropriate, in seeking an understanding of the physiological processes occurring in developing eggs, to distinguish between parthenogenesis and activation. A definite series of physical and chemical events ensue in eggs treated by agents inducing parthenogenesis. An apparently identical set of changes occurs at fertilization. This process which Needham (1932) has designated an opening of doors in the cell initiates the development of the ovum and makes of a static cell one capable of transformation. What happens subsequent to the activation process is often independent of the process itself. The probability of cleavage and the formation of a complete individual depends in part on the nutritional environment and the chromosome constitution of the activated egg.


The activation process in non-mammalian ova has been described in physico-chemical terms (see J. Loeb, 1913; F. Lillie, 1919; Just, 1928; Runnstrom, 1933; Whit aker, 1933; R. Lillie, 1934). There exists no similar information particularly for the ovarian eggs of mammals. The only established index of an activation of ovarian eggs is the described formation of the first polar body. It is conceivable that this represents the first step in an activation process that would go to completion if conditions were propitious. Perhaps the same pituitary stimulus that induces polar body formation might cause the formation of a cleavage spindle. The first cleavage spindles observed by Branca (1925) may then be considered the result of an activation process carried to completion because adequate pituitary stimulation was available. On this basis the liberation of ova from the ovary results in such a change of environment that the stimulus to completion of activation is ordinarily no longer available. Similarly mature ova retained in the ovary at the time of ovulation ordinarily degenerate either because the proper type of pituitary hormone is not active (c/. Hisaw's conception of the alternative action of follicle stimulating and luteinizing hormones) or because of the partition of the active hormone to other tissues {e.g., corpora lutea).


We may consider two further alternative explanations of the activation of ovarian eggs. It is possible that activation occurs in the ova of degenerating follicles because (1) the breakdown of cells near the ovum results in the release of activating substances or (2) the initial stages of atresia in the egg cytoplasm frequently involve structural changes in the egg cytoplasm which are identical with those changes occurring during normal activation.


According to the first of these two alternatives cell division stimulating substances are released as break-down products (Gutherz, 1925). That such substances are actually formed by mammalian cells has been attested by the study of the growth of tissue cultures (Carrel, 1924; Fischer, 1925) where they have been given the name trephones. Furthermore, signs of atresia in theca and granulosa cells are cytologically evident before signs of ovum breakdown. It has never been conclusively demonstrated, however, that trephones can activate ova (but see Haberlandt, 1922). On the other hand, it is conceivable that regardless of trephone action, the degeneration of follicle cells leads to a stimulating concentration of cytolizing substances {e.g., fatty acids which are known to act as activating agents) or even to a sufficient hypertonicity in the region of the ovum.


The second of these alternatives implies that ^Hhe opening of doors" occurring in normal activation is an aspect of degeneration. Atresia certainly involves changes in the colloidal structure of cells, and we have pointed out {vide supra) that definite changes in cortical structure mark the activation process. It is interesting, therefore, to note that the cytological appearance of the cytoplasm of retained ova with spindles is markedly similar to that of fertilized eggs. Thus the cytoplasm of unfertilized eggs have upon fixation a rough coarsely reticular appearance (see Figure 15 and Plate III, Fig. 4), whereas retained ova with spindles, like normally activated or fertilized eggs, have a uniformly granular cytoplasm (Figure 18).


Whether stimuli from degenerating follicle cells or endogenous structure changes are involved, it is evident that these factors are in turn conditioned by the supply of available hormone. Insufficient pituitary hormone results in the creation of ovum activating conditions. This is on the face of it, in direct contradiction of the first hypothesis which states that a supraliminal supply of hormone may also initiate activation. But this contradiction may be resolved if we consider that the same conditions may be created by either active pituitary stimulation or absence of it.

TABLE VII

The Development of Ovarian Eggs of the Rabbit in Media Containing Various Hormone Preparations. (From Pincus and Enzmann, 1935)

Number


Time of

OF

Medium

Results

CULTURING

Cultures


20 min.

14

Ringer-Locke + 1 drop beef pituitary

Vesicular tetrads formed in all cases


2 hrs.

11

Ringer-Locke -|2 drops beef pituitary

In some cases vesicular tetrads and some free tetrads were formed. Some formed polar bodies


24 hrs.

9

Ringer-Locke -f1 drop maturity hormone

Vesicular tetrads in all cases except 3 which had free tetrads


25 hrs.

4

Ringer-Locke -f 2 drops maturity

Vesicular tetrads in all cases

A.

hormone


25 hrs.

7

Ringer-Locke + 3 drops maturity hormone

Vesicular tetrads, free tetrads, structures resembling fusion nuclei


2 hrs.

18

Ringer-Locke

Vesicular tetrads and free tetrads


4 hrs.

3

Ringer-Locke

Free tetrads


6 hrs.

3

Ringer-Locke

Rudiment of first polar spindle


20 hrs.

IG

Ringer-Locke

Vesicular tetrads, free tetrads, fusion nuclei

24 hrs.

6

Plasma + 1 drop thyroxin


22 hrs.

4

Plasma + 3 drops thyroxin

22 hrs.

3

Phisma -|- 4 drops

All cultures showed about the

B

thyroxin

same phenomena which in

24 lirs.

8

Plasma -|- 6 drops thyroxin

cluded tetrad formation in all cultured eggs. In some

24 hrs.

4

Plasma -|- 8 drops thyroxin

of the cultures polar bodies formed, or the vesicular

20-24 hrs.

22

Plasma -|- 2 drops Ringer-Locke sol.

membrane dissolved


. 20-24 hrs.

8

Plasma -|- 6 drops Ringer-Locke sol.


It has been shown that pituitary hormones themselves do not act directly upon the ova (Pincus and Enzmann, 1935) by experiments in which ovarian ova with vesicular nuclei were cultured in media containing various pituitary extracts. The data of these experiments are summarized in Table VII-A. They show that in both the extractcontaining media and the extract-free media maturation proceeds at about the same rate. Furthermore thyroxin which causes a certain degree of maturation when injected in vivo (see page 51 above), causes in vitro no further degree of development than thyroxin-free controls (Table VII-B). The isolation of the ova from the normal follicular environment is sufficient to initiate activation. This implies that in preovulatory follicles maturation is caused by either (1) the mechanical separation of the ovum and its corona or (2) the removal of an inhibiting influence. Mechanical separation undoubtedly occurs (c/. Plate III, Figs. 8 and 9), but one cannot estimate the exact degree of isolation necessary to initiate maturation, for it is certain (Pincus and Enzmann, 1935) that maturation is initiated in ova still having strands connecting them to the follicular epithelium. In certain forms {e.g., man) the ova remain embedded in the cumulus mass till just before ovulation and the corona forms late. It is notable that Allen, Pratt, Newell and Bland (19306) were able to obtain only one maturation stage in some two hundred ova recovered from 3 to 20 mm. follicles. The writer (unpublished data) has observed one maturation occurring in a primate ovarian ovum, but when primate ovarian ova are cultured in vitro considerable nuclear activity occurs. During the first stages of pituitaryinduced maturation in the rabbit a secretion of secondary liquor folliculi is observed (Pincus and Enzmann, 1935). This secretion may remove an activation-inhibiting influence. The maturation observed in ova of atretic follicles may be due to a similar sort of secretion rather than to simple isolation of the ovum from its follicular epithelium.


Plate IV

Various stages in the development of the mature oocyte. (From the Archives de Biologie.)

Fig. 1, First maturation spindle — guinea pig. Fig. 2, Binucleated ovum, chromosomes oriented for the metaphase of a mitosis — guinea pig. Fig. 3, Binucleated ovum with formed maturation spindles — mouse. Fig. 4, Multinucleate cytoplasm — mouse. Figs. 5 and 6, Typical uninucleate cleaved ovocytes. Fig. 6 shows deutoplasmic extrusions — guinea pig.


On the basis of the foregoing considerations one might conceivably encounter occasional evidences of activation where alterations in normal hormone balance occur which are sufficient to cause a preponderating activation stimulus. Such may in fact be the basic cause of certain undoubtedly normal early development in ovarian eggs reported by a number of observers. In Plate IV, Figures 1 to 3 and Figure 1, Plate V, are presented various stages of pre-cleavage development found in ovarian eggs. The multinucleate condition of the egg of Figure 4 may be due to chromatin fragmentation, but the cleavages of the eggs of Figures 5 and 6 of Plate IV and Figures 2 and 3 of plate V are completely normal. It seems clear that at any one of these stages definite atresia of the ovum may set in, preventing further development. Similar arrests of development may occur in parthenogenetically activated invertebrate ova if the activating treatment is not carefully controlled (c/. Loeb, 1913; Just, 1928). Entrance into the cleavage process is likewise dependent upon a rather nice balance of developmental events. Furthermore, the processes involved in cleavage may indeed be independent of the activation process. Runnstrom (1933) has shown that sea-urchin eggs poisoned by monoiodoacetic acid can be fertilized but that segmentation soon ceases and ordinarily just before the dissolution of the nuclear membrane of the first cleavage division.


In later chapters we shall discuss further the problems involved in parthenogenetic activation. Now it is sufficient to indicate that there is a probability of activation of ovarian eggs but that a complete activation is dependent upon a balance of events which must presumably be rarely attained in the ovary. Even if the activation reaction proper occurs and segmentation ensues the probabilities that post-cleavage stages will be entered are made extremely small not merely because of the physical limitations imposed by the structure of the ovary, but because, as we shall demonstrate later (Chapter IX), the growth stage of the embryo is entered into only as the result of a definite hormonal stimulus during the luteal phase, and conversely is definitely inhibited by oestrin. It is therefore surprising that the blastula and neurula-like formations, described by Courrier (1923) (see Figures 4 to 7, Plate V) and Courrier and Oberling (1923) and the atypical ovarian embryos observed by Loeb (1932) should be found. The solution to the controversy concerning their exact nature must await evidence as to the possibility of their formation by experimental means.


Plate V

(Figs. 1 to 3 from the Journal of Anatomy; Figs. 4 to 7 from the Archives de Biologie.)

Fig. 1, Line drawing of a section through an atretic foUicle of the mouse. First mitotic anaphase. Cytoplasmic division not completed — mouse. Fig. 2, Typical 4-celled ovarian ovum — water vole. Fig. 3, Typical 2-celled ovarian ovum with intact zona — water vole. Fig. 4, Early blastocyst of ovarian ovum — mouse. Fig. 5, Many-celled blastocyst in ovarian ovum — guinea pig. Fig. 6, Multinucleate blastocyst-like ovarian ovum — mouse. Fig. 7, Blastocyst-like ovarian ovum — guinea pig.


It can be seen that the chance of atretic degeneration continually besets the ovarian egg. The evidence indicates this process can be avoided only if sufficient pituitary hormone is available to the ovary. There exists also the possibility that atresia is endogenous in the sense that the ovum as a cell attains a certain maximum degree of development and then inevitably goes down hill. Only the sudden intervention of ovulation and fertilization prevents this process. Such a conception is scarcely amenable to experimental verification chiefly because of the intimate association of the ovum and its follicle. Furthermore, signs of ovum degeneration are preceded by degenerative phenomena in the granulosa cells. If the granulosa and corona cells act as nurse cells to the ovum it is obvious that their behavior must largely condition the behavior of the ovum. Often the ovum becomes detached from the granulosa and corona radiata and floats practically free in the liquor folliculi. We do not know to what extent diffusion of a sufficiency of nutritive substances through the liquor folliculi is possible. The problem of the viability and senescence of the ovum still awaits experimental attack.



Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)
The Eggs of Mammals (1936): Introduction | The Origin of the Definitive Ova | The Growth of the Ovum | The Development and Atresia of Full-Grown Ova and the Problem of Ovarian Parthenogenesis | Methods Employed in the Experimental Manipulation of Mammalian Ova | The Tubal History of Unfertilized Eggs | Fertilization and Cleavage | The Activation of Unfertilized Eggs | The Growth and Implantation of the Blastodermic Vesicle | Summary and Recapitulation | Bibliography | Figures | Historic Disclaimer

Cite this page: Hill, M.A. (2018, October 23) Embryology The Eggs of Mammals (1936) 4. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/The_Eggs_of_Mammals_(1936)_4

What Links Here?
© Dr Mark Hill 2018, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G