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

ON THE DEVELOPMENT OF THE FISSURAL AND
ASSOCIATED REGIONS IN THE EYE OF THE CHICK,
WITH SOME OBSERVATIONS ON THE MAMMAL

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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114 I. C. Mann

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.