Paper - Development of the Mouse Gonads 3

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Brambell FWR. The development and morphology of the gonads of the mouse. Part III. The growth of the follicles. (1928) 103: 259-272.

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This historic 1928 paper by Brambell is the third in a series investigating the development of the mouse gonad.

See also: Brambell FWR. The development and morphology of the gonads of the mouse. Part I. The morphogenesis of the indifferent gonad and of the ovary. (1927) 101: 391-407.
Brambell FWR. The development and morphology of the gonads of the mouse. Part II. The development of the Wolffian body and ducts. (1927) : 206-219.
Brambell FWR. The development and morphology of the gonads of the mouse. Part III. The growth of the follicles. (1928) 103: 259-272.
Rowlands IW. and Brambell FWR. The development and morphology of the gonads of the mouse. Part IV. The post-natal growth of the testis. (1932) : 200-213.

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The Development and Morphology of the Gonads of the Mouse. Part III. The Growth of the Follicles

James Peter Hill (1873 - 1954)

By F. W. Rogers Brambell, Lecturer in Zoology, King’-s College, London.

Communicated by Prof. J. P. Hill, F.R.S. — Reoeived May 19, 1928.

From the Department of Anatomy and Embryology, University College, London.

1. Introduction

The present paper consists of a series of records of the growth of the oocyte and follicle in the ovary of the adult mouse. Wherever it has been possible, these records have been put in mathematical form. The results show clearly, amongst other things, that the major part of the growth of the Graafian follicle takes place after the contained oocyte has attained its maximum size. This fact is of considerable interest in connection with the evolution of the mammalian follicle and its physiological role.

The author would like to take this opportunity of expressing his thanks to “ Student ” for advice and criticism of the statistical treatment of the results, and to Prof. J. P. Hill, F.R.S., and Dr. A. S. Parkes for the interest they have taken in the work.

The histological expenses were defrayed by a grant from the GovernmentGrants Committee of the Royal Society, for which the author’s thanks are due.

II. Description

1. The Growth of the Oocyte

The smallest oocytes found in the adult mouse ovary are situated just beneath the germinal epithelium and are surrounded by a few flattened follicle cells. The oocytes only measure 13 μm in diameter, approximately. They are approximately the same size as the average of the primordial germ-cells found in and near the germinal ridge of the 10-days post-coitum embryo, which measure from 10-5 to 16-5 μm in diameter. The smallest oocytes in the adult ovary, enclosed in primordial follicles, are always situated just beneath the germinal epithelium, with at most three or four cells between. Their nuclei, however, never exhibit any contraction figures and are always in the dictyate condition.

Oocytes at all stages of growth between these small oocytes and the fullgrown oocytes, measuring approximately 70 μm in diameter, can be found in one ovary. It is impossible to ascribe a definite time limit to this growth stage, but it is probably fairly gradual. Once the oocyte has attained its maximum size it appears to remain, without growing more. until ovulation is almost due.

The nucleus increases in size with the growth of the oocyte. The Clianieters of a large number of oocytes and their nuclei were measured and the results treated statistically. The measurements were made from carnera.-lucicla drawings at known magnifications. The diameter of the outline of each ooc_\“cc and its nucleus was measured in two directions, at right angles to each other, and the average of each pair of mcasurenicnts was taken to be the true diameter. The results are shown in the form of a correlation table (Table I).

Table I



C! ‘E

{O O 3

N3 N3

2: -J O on ...a .— I-I '14 KS

n (3 10

,';Diamctcr of nucleus. IO N) CI v5 93 ‘I ha 1: rd

10 15 20 25 30 35 40. 45 50 55 60 I15 70 7;‘ 301,4 Diameter of oocyte.

The distribution of these data is not normal for two reasons : (1) The number of oocytes of a given size present in any ovary decreases as the size increases owing to degeneration taking place at all stages; and (2) oocytes of suitable sizes were selected for convenience. From these considerations it is obvious that the coeflicient of correlation will have no meaning apart from the data from which it has been derived. Since, however, the data were only selected in one direction — e.g., size of oocyte — the regression formula will supply a true value for the relation between the size of the nucleus and the size of the oocyte. The regression function, calculated from these data, is Y = 5-57 7 + (I-297 cc, where 3: is the given diameter of the oocyte and Y is the mean value of the diameters of the nuclei for each value of 1:. Entering the table oft (fisher (5) ) with 1 = 60-69, and n = 152, P is obviously much beyond 0-01 and therefore the regression is decidedly significant ; the growth of the nucleus and that of the oocyte undoubtedly proceeding simultaneously. This regression function is linear and is represented graphically in fig. 1, where the mean value of each array is also shown as an X.

Fig. 1.

2. The Growth of the Oocyte in Relation to the Growth of the Follicle

The diameters of a large number of follicles and their oocytes were measured. The method was the same as in the case of the oocytes and their nuclei. The results are shown in the form of a correlation table (Table II). These were treated as a regression, for the same reasons as in the previous section, of size of oocyte on size of follicle. The distribution seemed to justify dividing the correlation table into two parts, one covering the range of follicle diameters from O to 150 p. and the other from 150 to 650 n. The regression function for the first part. which is linear, is Y = 5-795 + 0-502 2:, where 1' is the given diameter of the follicle and Y is the mean diameter of the oocytes for each value of 1:. Entering the table of t (fisher (5) ) with t = 37-4, and n = 56, P is obviously much beyond 0-01 and therefore the regression is decidedly significant. The regression function for the second part, which is also linear, is Y = 69-54 — 0-0025 2:. Entering the table of t (fisher (5) ) with t = 1 -077, and 72. = 951, P is approximately 0-3 and therefore the regression is not significant (i.e., there is no significant alteration in size of the oocyte during the growth period of the follicle covered by the regression line). These regression functions are represented graphically in fig. 2. where the mean value of each array is also shown as an X . The two regression lines intersect at approximately 125 p. (diameter of follicle). These results show that the increase in the size of the oocyte bears a direct and significant relation to the size of follicle until it attains a size of approximately 70 p. in diameter, when the follicle is 125 p. in diameter. Subsequently, there is no significant growth of the oocyte, and the growth of the follicle may be said to be independent of it and can be represented by a horizontal line in the graph.

Table II.

4}- 15 10 so



2 I I-IGCVFQ sasssassa '¢.n£ooo3o«m°I-‘It!

ll: -1

2 _ \ 10 . . ' ' I ‘.

0 25 50 75 100 125 150 175 200 225 250 275 300 325 350 375 400 425 450 475 500 525 550 575‘ N0 525 Diameter of follicle. - '

Diameter oF oocyte

fiG. 2.

3. The Maturation of the Oocytes

The full-grown oocyte of the mouse with the nucleus in the resting dictynte stage. fixed in Bouin’s fluid, measures 70-96 5:. -3,; 0-25 μm in diameter. A reduction in size appears to occur during maturation. Ten oocytes, exhibiting the first polar spindle, from the ovaries of one mouse measured 66-9 μm in diameter, the largest being 71 p. in diameter and the smallest 63-5 p.. Three ova, from the Fallopian tubes of two mice, which in each case contained cl and 9 pronuclei unfused, and in which the second polar body had been extruded. measured 55.5, 56.0 and 57.3 μm in diameter respectively. These three ova had, however, been fixed in Carnoy’s fluid, and the difference. in fixation might account in part for the difierence in size. In any case the numbers observed are too small to supply a significant statistical dif‘iere11(-c_. although they suggest that a reduction takes place during the first maturation division and :1 further reduction during the second maturation division. The cytologit-al changes in the ovum of the mouse during maturation and fertilisation liave been described by Sobotta (11).

4. The Growth of the Follicle

The smallest oocytes, situated just beneath the germinal epithelium in the adult ovary, are only surrounded by a few flattened epithelial cellsmthe primordium of the membrana granulosa. These primordial follicles only measure about 17-5 μm in diameter. Slightly larger oocytes, about 14 μm in diameter, are surrounded by a single layer of more or less cubical epithelial cells, and are situated in or immediately beneath the tunica albuginea. Those follicles measure about 28 μm in diameter. The development of the various structures of the follicle is shown in tabular form in Table III (p. 264).

The follicles with a single layer of epithelium reach their maximum size at about 36 to 40 μm in diameter, with the contained oocytes 22 to 24 μm in diameter. By the time the oocyte has attained a size of about 30 μm and the entire follicle about 50 μm, the epithelium shows distinct signs of becoming doublelayered. The double-layered condition is fully established in follicles of 95 to 111 μm in diameter with oocytcs 55 to 60 μm. The follicular epithelium may now be considered to form a membrana granulosa. The growth of the follicle proceeds rapidly and changes from two to three cells thick by the time the oocyte has completed its growth and has attained a size of, on an average, 70 μm in diameter. "These follicles measure about 125 μm in diameter.

Table III

Diameter of follicle in Condition of oocyte. Condition of follicle. [1l . 17-5 13 p. in diameter Single layer of flIllt£'.n(!(l epithelial cells. 28 20 p. ,, ........ .. Single layer of cubical epithelial cells. 50 31 it n Follicular epithelium becoming two cells thick. 100 56 ,1 ,, .............. .. Membrana granulosn. two cells thick. Thcca interns beginning to differentiate. 125 Oocyte full grown. 70 n in . Membrana granulosa becoming three cells thick diameter ; and mitoses in it most frequent. 200 70 n in diameter Definite thecainternn. formed. Antrum first appears. 380 , 70 p. ,, ,...i Beginning of oestrous cycle ending in ovulation. 410 I 70 ,4 ,, .............. ..; (Estrus stimulation cfiected. Rapid growth-phase l starts. 530 I 70 p. ,, ............. ..' h‘e(-ondury liquor fulliculi appears. .\Iitosis in , mcmbrana granulosa stops. 550 [ lat polar spindle formed Oncyte in corona radiata floating free in the antrum.

About to Ovulate

Up to this time the growth of the follicle and of its oocyte have been correlated. The subsequent growth of the follicle, however, is entirely independent of the oocytc, which has reached its maximum size, and is due in part to the growth of the membrane granulosa and the development of the these. interna, but chiefly to the formation and increase in size of the antrum.

The epithelial cells of the membrane. granulosa grow rapidly by mitoses at all stages of follicular development. They exhibit mitoses even in the small follicles, where they constitute a single-layered epithelium. In follicles in which the membrana granulosa. is passing from the double- to the triple-layered condition many mitoses are present. They occur frequently in all stages until maturation is approaching. Mitoses then become less frequent, except in the region of the discus proligcrus, where mitotic figures are abundant, and, finally, in follicles containing mature oocytes in process of polar-body formation, practically none can be observed.

The bodies of Call and Exner, so common in the membrana granulosa of the follicles of man, cat, rabbit, etc, do not occur at all in .the mouse, nor is any comparable stellate arrangement of the cells cver observable.

The theca interna does not exist as a separate layer, in small follicles, which are surrounded by a coat of undifferentiated connective-tissue fibroblasts. Elements that would ultimately form the theca interns. can first be distinguished in this primitive theca of follicles approaching 100 μm in diameter. The cells are larger and more glandular in appearance than the surrounding fibroblasts among which they are scattered. The theca interns. cells and a few fibroblasts form a definite, if somewhat irregular, layer within the more fibrous theca externa, in follicles 200 μm in diameter.

At this stage the theca interna measures about 20 to 25 μm in thickness. It is rather irregular, but is, on the whole, as well developed on the side next the periphery of the ovary as on that away from it. At all stages it has numerous undifierentiated connective-tissue elements, as well as blood capillaries and lymph channels, scattered between the large, apparently glandular cells. It increases in thickness as follicular development progresses, except on the peripheral surface of the follicle. In the latter region it becomes thinned out as maturation is completed. In the follicle ready to ovulate it attains a maximum thickness of 30 to 40 μm on the side away from the periphery, but is very thin on the peripheral surface, where the membrana granulosa. is only covered by a. thin layer of fibroblasts, one or two cells thick, derived from the theca and tunica albuginea, and by the germinal epithelium. This peripheral thinning of the coat of the follicle allows of rupture being efiected more easily. The large flattened glandular cells of the theca interns exhibit many mitoses in the smaller follicles, but very few are present in the later stages of maturation.

The membrane. propria. is not well developed in the mouse, and consists of a light, fibrous network, between the membrane. granulosa and the theca interns.

The theca externa exhibits mitoses at all stages of follicular growth. It is thinner and more compact in the larger follicles, probably owing to stretching and compression exerted from within by the growth of the follicle.

The antrum first appears as an irregular fluid-filled cleft in the middle of the membrane. granulosa on one side of the oocyte, in follicles about 200 μm in diameter. This cleft enlarges as the follicle grows and comes to form a half-moon shaped cavity in the membrana granulosa with its concavity directed towards the oocyte. As maturation proceeds the antrum increases in proportion and becomes more or less the same shape as the follicle. with the discus proligerus and its contained oocyte projecting into it. The menibrana grauulosa enclosing the antrum, except on the side of the discus proligerus, is more or less uniform in thickness, varying from about 55 to 65 μm, at all stages of growth. The diameter of the antrum at right angles to the axis passing through the coyotes and the centre of the follicle can therefore be said to be roughly the diameter of the follicle less 120 μm This approximation obviously is more accurate for larger follicles, where the discus proligerus on account of its relatively smaller size does not seriously complicate the estimate.

5. The Growth of the Follicle in Relation to Oestrus

It is well known that the growth of the follicle is extremely rapid at the end, and that the main increase in its size takes place during a short period ending in ovulation. It has been shown elsewhere, in collaboration with Dr. Parkes (3), that the follicles, which will ovulatc at the following (estrous period, in the ovary of an unmated mouse are on an average only 380 p. in diameter at the beginning of the oestrous cycle. The follicles reach a maximum size of, on an average, 550 μm in diameter immediately before rupturing. Further, the follicles undergo comparatively little growth until 48 hours before the onset of the oestrous cornification, marking the period at which ovulation will take place. The growth, therefore. is increasingly rapid as oestrus approaches, and the follicles increase 45 per cent. in diameter in the last 48 hours.

A definite group of large follicles which will ovulate at the ensuing oestrous period can generally be distinguished in the ovaries of an unmated mouse. This group is, however, not very clearly defined, and sometimes the maturing follicles cannot be distinguished with certainty from those destined to ovulate at subsequent oestrous periods, if the ovaries were taken from an animal killed at the beginning of a cycle.

It was thought that several such groups of follicles, destined to mature at subsequent (estrous periods, might be present in the ovaries at one time. In consequence all the follicles measuring 75 μm in diameter and over in one ovary were measured and counted. The size distribution of these was such as to afford no prospect of demonstrating by statistical methods a series of folliclesizc groups in the ovaries of unmated mice. It may be assumed, as the contrary cannot be. demonstrated, that the follicles in the ovary of the unmated mouse are, as regards size, distributed at random, excepting those destined to rupture at the ensuing oestrus.

6. The Maturation of the Follicle in Relation to Oestrus

The follicles undergo various changes immediately before rupture. The ovaries removed from a mouse 6 to 26 hours before it came into oestrus (OVS 41) contained 12 large follicles, averaging 530 μm in diameter, the largest being 576 μm and the smallest 464 μm in diameter. These follicles differed little, except in size, from smaller ones. The oocytes had dictyate nuclei. The discus proligerus was still attached to the wall of the follicle, but in its neighbourhood the coagulated liquor folliculi, situated in the antrum and between the membrana granulosa cells, appeared more glairy and granular than elsewhere in the follicles, or than in smaller follicles. This thick liquor is that termed the secondary liquor folliculi. The ovaries removed from a mouse killed during late pro-oestrus or early oestrus (CLC 114) contained 11 large follicles, averaging 550 μm in diameter, the largest being 626 p. and the smallest 475 p. in diameter. The oocytes in all these follicles exhibited the first polar spindle, with the chromosomes in the equatorial plane or beginning to draw apart to either pole of the spindle. In these follicles the discus proligerus, containing the oocyte, had become separated from the wall of the follicle and floated free in the liquor-filled antrimi. The cells of the discus proligerus had become altered in character. They were arranged in a stellate manner around the oocyte and were drawn out in a radial direction forming a corona radiata. liquor folliculi was more abundant than in the previous example and was present between the cells of the discus. Coupled with these changes the thinning of the follicle wall at the periphery, described above, indicated that the secondary follicles were about to rupture.

The material from two mice exhibited ova in the Fallopian tubes. These ova had extruded the second polar body in each case and contained both male and female pronnclei approaching to each other. Ovulation in these had obviously occurred some hours previously, as the ova had reached the tubes and been fertilised. Both these animals had been killed on the morning on which the vaginal plug had been found. Mice usually copulate early in the night following the onset of (estrus. Further, oestrus usually commences in the evening. Consequently these animals cannot have been on oestrus more than 24 hours, and probably not so long.

Further, the ovaries of several mice killed during the first 12 to 18 hours after the onset of oestrus were available. All these exhibited young corpora lutea in various stages of formation from newly ruptured follicles. the tubes containing the ova of these were not available. to confirm the previous observations.

From these cases it is clear that ovulation in the mouse takes place during late pro~oestrus or very early oestrus. It probably occurs about the time when pro-oestrus changes into oestrus, and usually not more than 6 hours either side of this time. Within these limits a certain amount of variation may be expected to occur in difierent individuals and in different follicles in any individual. The material, however, is not sufficient to afford any further estimate of this variation. The actual size of the follicles at the time of rupture probably varies considerably also, as the case described (CLC 114) seems to indicate.

Unfortunately They serve, however,

7. The Number and Distribution of Mature Follicles in the Ovaries at Oestrus

The average number of follicles which mature in the two ovaries at each oestrous period can be estimated indirectly from the average size of litter born and the average. pre-natal mortality. Parkes (9) to be 6-34. It is obvious from these figures that at least seven ooeytes are matured at each oestrus.

The litter size has been shown by

The required figure can also be arrived at by counting the number of corpora lutea formed at each period, or, directly, by counting the number of maturing The latter method is somewhat uncertain immediately after an oestrous period, as the maturing follicles‘ are not sufficiently clearly defined by their sizes from the largest of the other follicles in serial sections of the ovaries.

follicles. The following table, however, contains the results from nine clear

Table IV.

Number-ui Reference number. maturing Distribution. follicles. C,‘-LC ll4 . . . . . ll 7/-I UV-*3‘ l25 .. .. . ll — (‘NS 41 ._ ., 12 cm OVH 39 in 5,‘-1 OVS 49 8 ——— ovs 90 .................... AV 3 4/4 ovs 52 .. . 9 0/3 (NS 40 .. .. .. 9 7/2 ovs 3o , W 7 41::

Eli ‘ i V 84- (‘I

These give an average of 9-3, which corresponds to the estimate arrived at from the size of litters. The problem of whether the maturing follicles are distributed at random between the two ovaries or tend to be equally distributed between them is of interest, but difficult to demonstrate on account of the amount of material required. In three of the seven cases recorded, the distribution was unequal.’ The material is insufiicient to show a significant difference from a. random distribution.

8. The Degeneration of Follicles

Many follicles of all sizes can be found degenerating in the ovaries of the mouse at any time after puberty and at all stages of the oestrous cycle. It is, however, very difficult to estimate this owing to being unable to tell for how long a degenerating follicle is distinguishable as such. In the case of the primordial follicles it is known (4) that they can completely disappear after treatment with X-rays in 24 to 48 hours. The degeneration of larger follicles is, however, much slower. In one typical ovary examined 128 normal follicles over 100 p. in diameter were counted and at least 66 follicles in process of degeneration which had been probably all over 100 p. in diameter before degeneration set in. It is, therefore, probable that a very large percentage of the follicles are eliminated at all stages up till the time of ovulation. This percentage appears to vary considerably in difierent individuals and to be much greater in poor conditioned and unhealthy than in sound animals.

III. Discussion

The Oocytes

The ovary of the adult mouse has never been observed to contain any oocytes exhibiting the prophase spireme and synaptic figures ((2) for previous literature). There can therefore be no doubt that oocytes do not pass through these stages in the adult mouse, as do those described in the Lemur by Gerard (6). This is held by many as definite proof that no neoformation of oocytes occurs in the adult mouse. Such a neoformation of oocytes from the cells of the germinal epithelium has been described by several authors, notably Allen (2), who admit that it takes place without going through the typical nuclear phases of synapsis. In the present paper no attempt has been made to solve this problem, owing to the inherent difficulties of estimating the "number of small oocytes in each of a large series of ovaries with sufficient accuracy to obtain statistically sound In this connection it is significant, however. that in the ovarian tissue regenerated in the mouse after complete double ovariotomy (10) oocytes were present but never exhibited the prophase figures.

Throughout the entire growth of the oocyte the nucleus is in the dictyate stage, and bears a constant relation to the size of the cell. it has attained its maximum size, appears to be able to remain for an indefinite time before it enters on the maturation stages. The material described supports the view that a slight decrease in the size of the oocyte takes place at the time of the formation of the first and second polar bodies.

Ovulation in the mouse appears to take place during late pro-oestrus or early oestrus. This-is earlier than Allen (1) considered to be the case, as he stated that it did not take place before the end of oestrus in the mouse, at the same time as Long and Evans (8) described it as occurring in the rat. The material described in this paper, however, admits of no other conclusion. i The number of follicles maturing in the nine pairs of ovaries dealt with averaged 9-3. Parkes (9) has shown that the average size of litter for the colony from which these are drawn is 6-34. It is therefore apparent that roughly two-thirds of the follicles which mature produce ova which survive till birth. This figure is slightly larger than that arrived at by Long and Evans (8) in the case of the rat, but is quite comparable. They found that the average number of corpora lutea produced in an animal at each (estrus was 10-8, while the average number of ova in the oviduct was 9-6. The average size of litter in their colony was 6-4.

The Follicles

The results obtained on the relative growth of the follicle and the contained oocyte show that a relation exists up till the time that the oocyte has attained its maximum size. This, however, takes place while the follicle is still comparatively small (125 p. in diameter approximately), and the subsequent growth of the follicle is not correlated with growth of the oocyte, which remains the same size. This conclusion, which has been quoted elsewhere (3), is of extreme importance in considering the morphological and physiological significance At the time when the oocyte has com pleted its growth, and therefore requires less nutrition, the follicle has a membrana granulosa composed of only three layers of cells, no traces of an antrum containing liquor folliculi, and scarcely any differentiated theca interna cells.

All the characteristics of the mammalian Graafian follicle are thus developed after the follicle has supplied the oocyte with the nutrition necessary for its growth. It may therefore be concluded that the mammalian Graafian follicle has evolved for some purpose other than the nutrition of the oocyte. Three possible explanations occur: the Graafian follicle as such has been evolved (1) as an endocrine organ, (2) to prepare for the rapid formation of the corpus luteuni, or as a mechanical adaptation to effect ovulation and the transference of the ova to the tube. Regarding the first of these possibilities the work of Parkes and the author (3) has shown that the Graafian follicle is not essential for the production of the hormone oestrin, which causes (estrus, and is probably not concerned at all in its production. This fact leaves us without any definite endocrine function to ascribe to the follicle.

The Monotremc follicle as shown by Hill and Gatenby (7) has no antrum, but the egg is large and yolk-laden. The fluid-filled antrum is thus associated only with the miorolecithal eggs of the higher mammals. It may be, therefore, that it has been developed as a mechanical means of effecting follicular rupture by internal pressure in microlecithal forms, where the ovum itself would find difficulty in bursting through the follicle on account of its small size. It is also possible, as has been suggested elsewhere (3), that the liquor folliculi is of assistance in washing the ovuni into the tube. At the time of ovulation the ovarian capsule and the tube in the mouse are distended with fluid. The amount of liquor folliculi liberated would not be suflicient to account entirely for this distention, but would probably materially assist in producing it.

Finally, the production of the large Graafian follicle may be a preparation for the formation of the corpus luteum. However, in the Monotremes. in which no antrum is formed, a corpus luteum is produced. In the latter case the ruptured follicle with its cavity is sufliciently large to develop speedily a large corpus luteum. This would scarcely be so in the higher mammals, unless the follicle grew beyond the size required to maintain the egg and attained the dimensions it does by the development of the large antrum.

At present it seems impossible to decide which of these theories is the true one. It may be that several functions are performed by the distention of the Graafian follicle with liquor folliculi and by the cells of the theca interns. Whatever these functions may be, the nutrition of the oocyte would not seem to be one of them.

IV. Summary

  1. During the growth stage, the diameter of the nucleus bears a direct relation to the diameter of the oocyte.
  2. The diameter of the oocyte bears a direct relation to the diameter of the follicle during the growth of the former. The oocyte attains its maximum size of 70 μm in diameter when the follicle is 125 μm in diameter.
  3. The main growth of the follicle, and the formation of the theca interns. and the antrum, take place after the oocyte has completed its growth.
  4. During the maturation divisions the oocyte is reduced in size. Fertilised ova only average 56 μm in diameter.
  5. The follicle grows rapidly, chiefly by enlargement of the liquor-filled antrum, during the two days immediately prior to the oestrous period and presumably in response to the production of mstrin.
  6. Ovulation takes place during late pro-oestrus or early (rstrus. The average number of follicles maturing at each oestrous period in one animal is 9-3.

V. Bibliography

(1) Allen, 131., Amer. Jour. Anat., vol. 30 (1922).

(2) Allen, E., ibid., vol. 31 (1923).

(3) Brambell and Parkes, A. S., Quart. Jour. Exp. Physiol., vol. 18 (1927).

(4) Brambell, Parkes, A. S., and Fielding, U., Roy. Soc. Proc., B, vol. 101 (1927).

(5) fisher, R. A., Statistical Methods for Research Workers, London (1925).

(6) Gerard, P., Arch. do Biol., vol. 30 (1920).

(7) Hill JP. and Gatenby JB. (1926) The corpus luteum of the Monotremata. Proc. Zool. Soc., London 96(3): 715-763

(8) Long, J. A., and Evans, H. M., Memoirs of the Univ. of California, No. 6 (1922).

(9) Parkes, A. S., Brit. Jour. Exp. Biol., vol. 4 (1926).

(10) Parkes, A. S., fielding, U., and Brambell, Roy. Soc. Proc., B, vol. 101 (1927).

(ll) Sobotta, J., Arch. f. Mikr. Anst., vol. 45 (1895).

Cite this page: Hill, M.A. (2019, January 24) Embryology Paper - Development of the Mouse Gonads 3. Retrieved from

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