Talk:Paper - On the development of the fissural and associated regions in the eye of the chick with some observations on the mammal (1921)

From Embryology


By I. C. MANN, M.B., B.S., Research Student in the Institute of Pathology and Research, St Mary’s Hospital

From the Department of Anatomy and Embryology

Ir is a well-known fact that in embryonic eyes, both avian and mammalian, the point of attachment of the optic stalk and of the early optic nerve is to the extreme lower part of the optic cup, while in the grown cyc it is practically half-way up the posterior surface of the globe. What then is the mechanism whereby the lower portion of the retina is formed? There is evidence to show that growth takes place below the level of the optic stalk, and that in the formation of the lower portion of the retina the choroidal fissure and parafissural regions are concerned. The closure of the choroidal fissure takes place very early in the mammalian eye, but in the large eye of the chick embryo the process is relatively slower and can be more easily observed.

In the eye of the chick embryo the choroidal fissure is at first very short and directed vertically downwards. Its margins apparently come together first in the intermediate portion, leaving the proximal part open for the ingrowing vascular mesoderm. This mesoderm, which in differentiation very soon shows one or two definite thin-walled blood vessels, at first occupies the whole of the interval between the intermediate closed portion and the upper end of the fissure, and, after traversing the lower part of the globe, passes out again at the distal opening in the fissure at the pupillary margin.

The growth of the lower part of the retina apparently takes place by extension of the margins of the cleft and neighbouring areas in the form of two processes or cornua which extend downwards, curving of course outwards with the retinal concavity to reach the pupillary margin. Further, it appears probable that the growth of these two cornua is not exactly equal, the posterior or malar one increasing slightly more rapidly than the anterior, with the result that the line of the fissure becomes altered as growth proceeds. The direction is at first vertically downwards, but in the adult bird the line of the fissure, which is represented by the line of nerve fibres entering the so-called cauda of the nerve, runs downwards and forwards. In a series of chick embryos of increasing age this alteration in direction can be seen to take place gradually, the angle decreasing in successive specimens from a right angle in the earliest embryos examined to about 70° with the horizontal in the adult bird. It is

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also noteworthy that the nerve fibre layer of the developing retina appears first in the region above the optic stalk, namely in the oldest part of the retina, and thence extends gradually downwards on either side of the fissure, the area possessing nerve fibres being at one stage slightly more extensive on the malar side of the cleft than on the nasal.

The adult bird, however, differs from the mammal in that in the former the blood vessels enter the eye some distance below the nerve attachment, and also in that some of the nerve fibres pass out of the globe below the nerve attachment and run up to this on the back of the eye: these constitute the cauda, The fissure in the bird, however, as will be apparent later, originally exists proximal to the point of entry of the vessels, and, as in the mammal, the upper end of the fissure is included in the nerve attachment.

At an early age in the chick, possibly as a result of quicker growth of the inner, non-pigmented, layer of the optic cup, this layer becomes everted, so to speak, in the lips of the fissure. This condition is shown in fig. 1, which represents a section through the eye of a chick embryo of about four days. The fissure is still open in its entire length and, though very little pigment is as yet present in the outer layer of the cup, the everted portion of the inner layer at the margins of the cleft can be recognised by its similarity in thickness and type of cell to the true inner layer. This eversion occurs in the upper part of the cleft first, and is always more marked here. The everted area elongates with the elongation of the fissure, but not co-extensively with it and so never reaches the pupillary margin. At first the entering vessels occupy the whole of the region of the fissure bordered by this everted area, but later, as the margins of the fissure come together, the entering vessels lie towards the lower end of the area. From their point of entrance they pass forwards in the vitreous, forming a vascular septum stretching across the lower part of the globe to their original point of exit from the cleft just below the pupillary margin. This distal portion of the fissure soon closes and the vessels are cut off here and gradually become shorter. Their subsequent fate will be discussed later.

The upper part of the cleft must now be considered. It is easily seen that when this upper part closes fusion takes place, owing to the eversion just, described, between two portions of the non-pigmented inner layer only. After obliteration of the cleft there remains an area of non-pigmented (originally inner) layer on the outer surface of the globe, this area being directly continuous at its edges with the true outer pigmented layer some little distance away from the fissural line. This condition is shown in fig. 2, which is a transverse section (from a slightly older chick) through a portion of the back of the globe including the margins of the cleft in the region between the point of attachment of the optic stalk above and the entering vessels below. It will be seen that fusion takes place between comparatively large areas of inner layer, so that two projections or ridges are formed by the heaping up of this layer, one, anterior, projecting into the globe, the other, more marked, on the postcrior surface, continuous at its base with the pigment layer. Fig. 3 shows the mode Fissural and Associated Regions in the Eye of the Chick 115

Figs. 1-5. Sections through embryonic chick eyes. Fig. 6. Adult hen. Figs. 7 and 8. 15 mm human embryo. (From camera lucida drawings.) 116 I. C. Mann

of fusion of the lips of the cleft in the region of the entering vessels. Ht will be seen that the overgrowth of the inner layer is not sufficiently marked here to give rise to definite eversion and the formation of a posterior ridge, but that it is great enough to form the anterior projection and that here, as in fig. 2, the fusion occurs between two non-pigmented arcas only. The anterior prominence fades away below the vessels. Thus it comes about that in a fresh, chick embryo the line of the fissure stands out as a white streak on the superficial surface of the large pigmented eye. Developing nerve fibres adjacent to the sides of the fissure will grow into this posterior non-pigmented area since it is in origin directly continuous with the fibre-bearing inner retinal layer. This morphological continuity is well seen in early chicks where there is some attempt at the formation of a rod and cone layer to be seen in the everted portion. This is indicated in fig. 2. This appearance is of short duration since the cells are soon obliterated by the ingrowing nerve fibres, which become visible as bundles running up on the back of the globe to the nerve attachment, thus later forming the cauda of the adult nerve.

Fig. 4 shows a later stage through the same region as in fig. 2. The nerve fibres can be seen passing into the projection on the posterior surface, which now consists of bundles of fibres forming the cauda and running up to the nerve attachment.

These phenomena of closure as seen in the upper part of the cleft are intimately connected with the development of the pecten and some mention must be made of this in explaining the subsequent fate of the margins of the fissure. It has already been shown that the posterior projection of the nonpigmented layer in the upper part of the fissure provides the path for the fibres of the cauda of the nerve.

The fate of the anterior ridge remains to be dealt with. The lower portion of this, below the entering vessels, very soon after fusion of its two component lips and before the appearance of nerve fibres in this region, becomes flattened and takes on the character of the retina on cither side of it and no trace of the situation of the ridge can be subsequently demonstrated.

The upper portion (fig. 2), which will be referred to as the crista intraocularis, behaves differently. When the developing nerve fibres grow towards the region of the cleft (figs. 2 and 4) they do not reach the posterior everted projection by remaining on the surface and entering along the line of fusion, but they begin to sink into the substance of the inner (retinal) layer along the base of the crista and so by taking a more direct route they cut off, as it were, the portion of the inner layer which forms the ridge, and separate it from the deeper strata. The cells of the crista intraocularis never show any attempt at differentiation into nervous retinal elements. At first (before the appearance of the nerve fibre layer) the tissue appears to be spongioblastic in nature. Later, as the ridge becomes cut off by the ingrowing nerve fibres, it takes on a more reticular appearance, the cells becoming smaller and somewhat stellate and the whole structure appearing as a loose meshwork of cells and fibrils covered and Fissural and Associated Regions in the Eye of the Chick 117

limited on its free or vitreous surface by the membrana limitans interna and in relation on the inner side of this again with the hyaloid membrane, which is always firmly adherent to the ridge.

By this time a change has taken place in the arrangement of the blood vessels entering the eye. The vascular septum which at first passed through the lower part of the globe entirely disappears. The proximal portion of the vessel however remains and now enters the eye at the lower end of the crista intraocularis. This ridge of loose reticular tissue, described above, now becomes vascularised by branches of the vessel running in its substance towards the upper end. These branches increase in number and the crista becomes more marked and develops a sharp apex. The ridge now shows in its lower part as the primitive unplicated pecten. Growth proceeds from below up and the pecten develops as a septum growing out into the vitreous (the hyaloid membrane being always firmly attached to its sides and apex) and consisting of ramifications of the proximal part of the original choroidal vessels enclosed in a loose stroma, neuroglial in nature, derived from the portion of the fused lips of the fissure cut off by the growing nerve fibres. This condition can be seen in fig. 5, which should be compared with the preceding figure, where the precursor of the pecten can be clearly seen in the form of the crista intraocularis. Later the pecten grows rapidly, becomes many times folded upon itself in a complicated manner, and pigment is developed in it. Fig. 6 shows a section through the extreme upper end of the pecten in an adult hen’s eye. It can be easily seen that it occupies the position of the crista intraocularis in the embryonic cye and that its “roots,” if the term may be used, are directly continuous with the supporting neuroglial septa of the optic nerve, in which, however, there is no pigment. It is in this way easy to understand that the peeten ex origine is attached along a line extending between the optic nerve and the entering vessels.

Examination of various embryos shows that the earlier stages in development of the chick’s eye have their parallel among the mammalia. The eversion of the inner layer in the upper part of the cleft occurs in mammals but to a much less extent than in the bird. The position of the arteria centralis retinae shows that this eversion must be of the lips of the fissure. Figs. 7 and 8 show the condition in the 15 mm. human embryo. Fig. 7 shows the cleft with the entering vascular tissue. It will be seen that the out-turning of the inner layer is marked. Fig. 8 shows the condition immediately below that shown in fig. 7 in the same embryo. The two everted inner layers have come together and fused, forming a small mass of non-pigmented cells continuous with the outer pigmented layer (the parallel of the larger structure in the chick). These nonpigmented cells do not appear connected with the inner layers here since in man no nerve fibres grow into this everted region and no cauda is formed to the optic nerve.

The condition can be seen best in human embryos of 18 mm. and 15 mm. It is extremely small in the 16 mm.embryo and in the 18 mm. it has practically 118 I. C. Mann

disappeared. It is very well marked in carly mouse embryos. There is no trace of the formation of a true crista intraocularis in the mammalian eye. It is true that when the inner layers of the retina fuse below the arteria centralis retinae in the mammal the site of fusion remains for a very short period as a slight projection into the vitreous which, like the similar area below the vessels in the chick, soon becomes flattened and indistinguishable from the retina on either side of it. There is, however, no sign of a crista above the vessels, and the nerve fibres pass into the nerve head on the inner surface of the inner layer and do not sink deep to it in any place.

The possible causes of this difference of behaviour of the avian and mammalian cleft margins are of course somewhat obscure, but may be associated with relative differences in dimensional growths of the lower portions of the retinal fields and also with the relation in time between the appearance of nerve fibres in various areas and the closure of the cleft. It is hardly necessary to say that the eversion of the inner layer must occur while the cleft is, potentially at least, still open.

In conclusion, I wish to express my thanks to Professor Frazer both for the loan of much valuable material and for his encouragement and advice in the preparation of this paper.