Ocular pigmentation in white and Siamese cats - Journal of Vision
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Ocular pigmentation in white and
Siamese cats
L. N. Thibos, W. R. Levick, and R. Morstyn
Ocular pigmentation in white cats with blue and. yellow eyes and in Siamese cats was examined
ophthalmoscopically and histologically. Yellow-eyed, white cats had. entirely normal ocular
pigmentation. Blue eyes of white cats had. normal pigmentation of the iridial and. retinal
pigment epithelia but no stromal pigmentation of the iris or choroid. This deficit is apparently
due to the absence of stromal pigment cells, certainly in the iris. As a general rule, the blue eye
of white cats had no tapetum. Siamese cats had reduced pigmentation of the iridial and retinal
pigment epithelia and no stromal pigmentation of the iris or choroid. The lack of pigmentation
is apparently due to the inability of stromal pigment cells to produce pigment, certainly in the
iris. We conclude that the abnormality of visual pathways previously described, in the Siamese
cat is not due simply to a deficiency of pigment in cells of neural crest origin.
Key words: ocular pigments, white cats, Siamese cats, iris pigment,
choroid pigment
v3iamese and white cats are two breeds This report describes the extent of ocular
which have a deficiency of coat pigmentation pigmentation in white cats as compared with
and which can also have reduced ocular pig- Siamese and normally pigmented cats. Sev-
mentation. The comparative details of this eral of the animals used in these experiments
hypopigmentation are of interest because the were also subjects in neurophysiological in-
Siamese cat suffers from an abnormal visual vestigations of the visual pathways which are
pathway 1 " 3 yet the white cat does not. 4 Al- described elsewhere. 4
bino individuals of other mammalian species
have pathway abnormalities similar to those Methods
in the Siamese cat, and the suggestion has Ophthalmoscopic observations of six adult white
been made that the cause might be specifical- cats (A through F) of undetermined genetic con-
ly related to the amount of pigment in the stitution were made after each animal was pre-
retinal epithelium. 5 ' 6 pared for neurophysiological recordings. The
pupil was dilated with atropine drops (1%), and a
zero-power contact lens was fitted. Additional ob-
servations were made on six white, five Siamese,
From the Department of Physiology, John Curtin School and one solid black cat (cats G through S). Color
of Medical Research, Australian National University, photographs of the fundus and iris were taken with
Canberra, Australia. a Zeiss fundus camera and Kodacolor 400 film.
L. N. Thibos was supported by a Postdoctoral Fellow- Upon completion of neurophysiological exper-
ship of the U. S. Public Health Service. R. Morstyn
iments, a dose of about 30 mg of pentobarbitone
was a Vacation Scholar of the Australian National Uni-
versity.
per kilogram of body weight was administered in-
Submitted for publication Dec. 27, 1978. travenously, and the eyes were enucleated. Each
Reprint requests: Dr. W. R. Levick, Department of eye was then hemisected at the pars plana, the
Physiology, John Curtin School of Medical Research, vitreous and lens were discarded, and the remain-
Australian National University, P.O. Box 334, Can- der was fixed in 10% neutral buffered formal
berra City, A.C.T. 2601, Australia. saline.
0146-0404/80/050475+12$01.20/0 © 1980 Assoc. for Res. in Vis. and Ophthal., Inc. 475
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476 Thibos, Levick, and Morstyn May 1980
Fig. 1. For legend see facing page.
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Number 5 Ocular pigmentation in cat All
To get satisfactory iris preparations, animals G illumination the iris had a translucent to di-
through R, which were not part of neurophysiolog- aphanous appearance, quite different in side-
ical experiments, were given 2 drops of 0.5% by-side comparison with irides of white cats.
physostigmine to contract the pupil. A lethal dose Fundus. The dominant feature of an ordi-
of pentobarbitone was administered, and the eyes nary pigmented cat's fundus is the yellow-
were enucleated and fixed as described above.
green tapetum which is surrounded by very
Before the histological preparation was begun,
fundus tissue was sandwiched between slices of
dark pigmentation. Although the precise size
fixed cat liver to minimize detachment of the ret- and shape of the tapetum varies somewhat
ina from the choroid. Tissues were embedded in from cat to cat,7 it is possible to predict the
paraffin, and 5 /u,m sections were prepared with location of the tapetum with acceptable reli-
hematoxylin and eosin stain. In some preparations ability. We shall refer to this fiducial region
melanin pigment was bleached by treatment with where one expects to find a tapetal reflection
0.1% potassium permanganate followed by 1% as the tapetal zone. The statements which
oxalic acid. Photomicrographs were taken with a follow are based upon complete ophthalmo-
Zeiss photomicroscope. scopic and microdissection surveys of the
entire fundi supported by selected fundus
Results photographs.
Ophthalmoscopic and microdissection ob- The fundi of yellow-eyed white cats had
servations. A summary of the gross appear- the same appearance as those of ordinary
ance of the irides and fundi of the 18 subjects pigmented cats. A yellow-green reflection
is given in Table I. from the tapetal zone and the retinal blood
Iris. Color photographs of the living cat iris vessels within this region were clearly visible
are given in Fig. 1, A, for a yellow-eyed ophthalmoscopically (e.g., upper part of Fig.
white cat and in Fig. 1, C, for a blue-eyed 1, B). The shape and size of the tapetum was
white cat. Dissection of the eyes of white cats within the normal range.7 The nontapetal
revealed the posterior surfaces of the irides to zone appeared dark brown (e.g., lower part
be as darkly pigmented as in the ordinary of Fig. 1, B) due to the presence of pigment
pigmented cat. Side-by-side comparison un- in both the retinal epithelium and choroid as
der transillumination showed that the yellow observed by microdissection. However, in
and blue irides of white cats were each as eight of 12 eyes there were horizontally elon-
opaque as the yellow iris of a black cat. gated patches of inferior fundus about 5 to
The blue iris of a seal-point Siamese cat is 10 mm wide and 2 to 4 mm high where
shown in Fig. 1, E. The posterior surface of choroidal pigment was completely missing.
the Siamese iris was not as heavily pigmented Apart from these patches, the choroid was
as in the ordinary pigmented cat, appearing a equally heavily pigmented inside and outside
dark chocolate brown in the seal point and a the tapetal zone.
lighter brown in the lilac point. Under trans- The fundus of the usual blue-eyed white
Fig. 1. Iris and fundus of the living cat eye. Shown are yellow-eyed white cat iris (A) and
fundus (B), blue-eyed white cat iris (C) and fundus (D), and seal-point Siamese iris (E) and
fundus (F) (left eye of animals Q, R, and S, respectively). The darkly pigmented pupillary ruff
of the epithelium, located at the pupil margin, is more evident in A and C than in E. Note the
translucent quality of the Siamese iris. Fundus photographs all show the inferior border of the
tapetal zone with the retinal blood vessels exiting from the optic nerve head in the upper left of
the picture. Each field subtends about 30° of visual angle and each is centered approximately
15° below and 7° nasal to the center of the area centralis, so as to show parts of both tapetal and
nontapetal zones. B has the appearance of the ordinary pigmented cat's fundus. D lacks both
tapetum and choroidal pigment, thereby revealing choroidal blood vessels. Clumps of retinal
epithelial pigment are evident at the bottom of D. Because of the absence of a reflecting
tapetum, the exposure for this photograph had to be increased substantially relative to B and
F. F has a tapetum, dilute epithelial pigment, but no choroidal pigment; thus the choroidal
vessels are visible below the tapetal zone.
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478 Thibos, Levick, and Morstyn May 1980
Table I. Summary of macroscopic appearance of ocular pigmentation
Cat identification /breed
G A F H Q B D E L C I p R J M N s K
Eye Bl W W W
w W W W W W w- w W SS SS SS SS LS
Iris color Y Y By Y By B B B B B B B B
R Y Y Y Y Bv B B B B B B B B B
Iris epithelium L 0
o o o o
R o 0 o o o
Choroid L Of o o o 0 o o o o
R o o o o o o o o o
Tapetum L O o o o
R o o o o
Retina epithelium L O G O O O
outside tapetal
zone R O O O O O
W = white cat; Bl = black cat; SS = Seal-point Siamese cat; LS = Lilac-point Siamese cat. Letter O not used for
identification of cat.
Y = yellow appearance; B = blue appearance; By = blue with yellow sector.
Key: • Pigment (or tapetum) present; O pigment diluted; O pigment (or tapetum) absent.
'"Absence of pigment in a portion of inferior fundus.
tQuadrantic sector of pigment in temporal midperiphery.
cat was strikingly different from that of the same as for the white cats described above.
ordinary pigmented cat.8- 9 There was no However, side-by-side comparison between
bright yellow reflection from the tapetal fundi of the Siamese and blue-eyed white
zone, nor was there any choroidal pigmenta- cats, neither of which had choroidal pigment,
tion. Hence in vivo the tapetal zone had the showed that the white cat's epithelial pig-
appearance of a jungle of red blood vessels ment was significantly darker. Even at the
(e.g., upper part of Fig. 1, D). Microdissec- border of the tapetal zone where the epithe-
tion of the fixed eyecup showed complete lial pigmentation just began, it was observed
lack of choroidal pigmentation. There were that the pigment clumps in the white cat
the following exceptions. In three eyes a pre- were darker than pigment in any part of the
dominantly blue iris was partly yellow; in two Siamese retinal epithelium. This dilution of
of these eyes the fundus had both tapetum epithelial pigment was quite definite in the
and choroidal pigment. In all the blue-eyed seal-point Siamese and even more obvious in
white cats the pigment of the retinal epithe- the lilac-point.
lium was present outside the tapetal zone but Histological observations
not within, just as in normal eyes. Pigmenta- Yellow iris. A cross-sectional view of the
tion is shown in the lower part of Fig. 1, D, yellow iris taken from a black cat is shown in
partly obscuring the choroidal blood vessels. Fig. 2, A, and from a yellow-eyed white cat in
The Siamese fundus in vivo showed a Fig. 2, B. The pigmentation of the white cat's
slightly desaturated tapetal reflection (e.g., iris is the same as for the black cat's iris: both
upper half of Fig. 1, F) and outside the have heavily pigmented epithelial cells plus
tapetal zone appeared reddish brown10 (e.g., light brown pigment cells of the stroma. The
lower part of Fig. 1, F). Microdissection stromal pigment is in the form of long thin
showed that there was no choroidal pigmen- filaments similar to that found in rhesus mon-
tation. Visibility of the tapetum was reduced key iris stromal cells11 known to be true mela-
in the fixed eye cup, probably because the nocytes.12' 13 Thus it is likely that the cat's
absence of choroidal pigment led to increased stromal pigment cells are also melanocytes.
amounts of scattered light. The distribution A magnified view of individual stromal
of pigment in the retinal epithelium was the pigment cells is given in Fig. 3, A. Perikaryal
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Number 5 Ocular pigmentation in cat 479
B
100 y
Fig. 2. Cross-sections of irides from black (A), yellow-eyed white (B), blue-eyed white (C), and
Siamese (D) cats (animals G, H, I, and K, respectively). Specimens oriented with posterior
(epithelial) surface to left, anterior (stromal) to right. Magnification bar (100 ju,m) is common to
all. Pigment cells (PC) and pupillary ruff(R) are labeled in A only.
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480 Thibos, Levick, and Morstyn May J980
A B
Fig. 3. Tangential sections of irides of yellow-eyed white (B), blue-eyed white (C) and Siamese
(D) cats (same animals as in Fig. 2). Presumed pigment cell nuclei (PN) indicated by arrows.
Magnification bar (100 /Am) in B applies to B to D only. A, High-magnification view of three
pigment cells found at various locations of the iridial stroma in yellow-eyed white cat of B.
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Number 5 Ocular pigmentation in cat 481
Fig. 4. Fundus cross-sections in nontapetal region approximately 5 to 7 mm below the area
centralis in black (A), yellow-eyed white (B), blue-eyed white (C) and Siamese (D) cats (animals
G, H, I, and J, respectively). Structures indicated are photoreceptors (R), retinal epithelium
(E), choroidfCj, sclerafSJ, and blood vessel (B). Magnification bar (100 JLUTI) is common to all.
Separation of layers is artefactual.
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482 Thibos, Levick, and Morstyn May 1980
Fig. 5. Fundus cross-sections in tapetal region approximately 3 mm above the area centralis.
Animals used and key to structures indicated are as in Fig. 4. Tapetum (T) is also shown.
Magnification bar (100 fxm) is common to all.
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Number 5 Ocular pigmentation in cat 483
shape varies from nearly circular to long and region about 7 mm below the area centralis.
slender. A constant feature of these cells is Pigmentation of choroid and retinal epi-
the large, darkly stained, oval nucleus. The thelium in the nontapetal zone for a black cat
mean of the minimum and maximum nuclear is shown in Fig. 4, A, and the yellow-eyed
diameters determined for 20 cells ranged white cat in Fig. 4, B. Epithelial pigment
from 4.75 to 7.25 /am and averaged 5.5 /xm. thickness was in the range of 10 to 20 /Am in
Such nuclei were found only within the pig- these cats. A heavy infiltration of pigment
mented cells of the stroma. obscured the nuclei of the choroidal cells, but
Stromal pigment cells tended to be con- bleaching revealed the nuclei to be of vari-
centrated on the anterior surface of the iris. A able size and shape with no unambiguous
tangential section made parallel to the iris identifying characteristics. The thickness of
surface therefore revealed a large number of the choroid was due mainly to blood vessels
pigment cells for both black and yellow-eyed rather than the thin pigment cells.
white cats (Fig. 3, B). The greatest density of Within the tapetal zone of the black (Fig.
pigment cells was found at invaginations and 5, A) and yellow-eyed white (Fig. 5, B) cat
at the margin of these sections, which was the fundus the retinal epithelium was devoid of
most anterior portion of the tissue. pigment, and the large, roughly circular nu-
Blue iris. Cross-sections of the blue-eyed clei of this single-cell layer were evident. The
white cat's iris showed a normal, heavily tapetal cells were easily recognized by their
pigmented epithelium (Fig. 2, C). No pig- large nuclei, elongated perikaryon, regular
mented cells were found in tangential sec- array, and particular coloration. The choroid
tions of iris (Fig. 3, C). We ruled out the was equally heavily pigmented in the tapetal
possibility that such cells were present but and nontapetal zones.
unpigmented, as suggested by Lauber,14 be- Fundus of the blue eye. Outside the tapetal
cause none of the stromal nuclei had the zone the blue-eyed white cat's fundus (Fig.
quantitative characteristics described above. 4, C) had heavily pigmented retinal epithelial
Pigmentation in the Siamese blue iris was cells. Above the area centralis within the
distinctly different from that of the blue-eyed tapetal zone the retinal epithelium was un-
white cat. The layer of pigment within the pigmented (Fig. 5, C) as in the ordinary pig-
epithelium was thinner, and the granules mented cat, but tapetal cells were absent en-
were less densely packed, particularly in the tirely. There was no choroidal pigmentation.
lilac-point animal. Consequently individual Because no unique features of choroidal pig-
pigment granules could be observed, and ment cells had been found in the ordinary
the normal pupillary ruff was hardly evident pigmented cat, we were unable to determine
(Fig. 2, D). The stroma was not pigmented, whether in the blue-eyed white cat the pig-
but contrary to the situation in the blue-eyed ment cells were present and unpigmented or
white cat, the pigment cells were evidently completely absent.
present. This conclusion is based on the The Siamese cat had a thinner than normal
tangential section of Fig. 3, D, which shows layer of pigment in the retinal epithelium in
many large oval nuclei having the expected the nontapetal zone (Fig. 4, D). From the
quantitative characteristics. edge of the tape turn to the ora terminalis, the
Fundus of the yellow eye. The comparison maximum thickness of the epithelial pigment
of pigmentation in different eyes is most layer in the seal-point retina was 5 (xm and in
straightforward if one avoids the margin of the lilac-point 3 fxm, considerably less than in
the tapetal zone where the thickness of epi- the ordinary pigmented cat. Within the
thelial pigment varies. Accordingly, the data tapetal zone there was no epithelial pigment
presented below for the tapetal zone are from and the tapetal cells appeared normal. Cho-
the region about 3 mm above the area cen- roidal pigmentation was completely absent
tralis and for the nontapetal zone is from the throughout the fundus, but it could not be
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484 Thibos, Levick, and Morstyn May 1980
determined whether the pigment cells were white also carried the gene pattern for
absent altogether or present but devoid of piebald spotting of the eye. White spots
pigment. would be undetectable in the completely
white hair and pink skin caused by dominant
Discussion white, but the edges of a spot might be re-
The results of this study are best summa- vealed by the ocular pigment.
rized in relation to the postulated embryolog- Tapetum lucidum. The results obtained
ical source of the various types of ocular pig- from blue-eyed white cats have shown that
ment cells. This is not known specifically for the usual deletion of pigment from the retinal
the cat, but the following description is epithelium within the tapetal zone is not
common to other mammals,15' 16 birds,17 and under direct tapetal control, since in these
amphibia.18 Pigment cells of the iris and cho- cats the tapetal cells were absent but the dis-
roidal stromata are derived from cells which tribution of retinal epithelial pigment was
migrate from the neural crest. The tapetal normal.
cells of the cat are likely to be modified cho- Bernstein and Pease19 have suggested that
roidal pigment cells19 and hence also of tapetal cells are modified choroidal melano-
neural crest origin. On the other hand, the cytes. The Siamese has heretofore been in
pigment epithelia of the retina and iris are apparent contradiction to this hypothesis,
products of the embryonic eye cup. since choroidal pigment is missing yet the
Our results show that the yellow-eyed animal has a normal tapetum. The inconsis-
white cat has normal ocular pigmentation but tency is resolved if the present results on iris
the blue-eyed white cat lacks pigment in the tissue are generalized to include choroid. We
iridial and choroidal stromata. The basis of may suppose that unpigmented choroidal
the deficit in the blue eye appears to be the pigment cells are likely to be present in the
absence of the pigment cell itself. Presum- Siamese cat and therefore the derivative ta-
ably the neural crest cells either failed to mi- petal cells would be present as well. If this be
grate to the ocular tissue or failed to differ- true, it would imply that functional tapetal
entiate and survive as uveal pigment cells. rods, which are the basis of light reflection
The Siamese cat is also deficient in ocular phenomena,21 are not dependent upon mel-
pigment but in quite a different way. First, anin production.
there is a relative diminution of pigmentation Genetics. The all-white coat of the white
of the iridial and retinal epithelia. Second, cat is inherited as a dominant character8'20"22
the common lack of pigmentation in iridial and therefore cannot be the result of the ac-
and choroidal stromata is associated with the tion of an allele at the albino locus.23 There
presence of unpigmented pigment cells, cer- has been only one report of an albino cat,24
tainly in the iris and possibly also in the but it is commonly believed that the Siamese
choroid. breed represents an imperfect form of albi-
In summary, the blue-eyed white cat lacks nism, as first suggested many years ago.25' 26
a particular cell type, whereas the Siamese is The evidence for this view is that (1) Siamese
defective in pigment production. is a recessive characteristic2' resulting in
There were exceptions to the above gen- hypopigmentation and (2) the pattern of
eralizations. Three of 12 blue irides of white thermolabile coat pigmentation in the Sia-
cats had yellow sectors, and in one of these mese cat resembles that in the Himalayan
eyes there was a patch of choroidal pig- rabbit,28' 29 the gene of which is known to be
mentation. In eight of 12 yellow eyes of white allelomorphic with the albino gene.27
cats the choroidal pigmentation was incom- The cause of the lack of pigment in albino
plete. This heterogeneity might indicate the animals and some albino humans appear to
presence of piebald spotting in the eye. It has be a failure of individual melanocytes to pro-
long been suspected20 that a blue eye would duce pigment because of default of the en-
appear if a cat carrying the gene for dominant zyme tyrosinase.l6- 30> 31 A piebald white spot,
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Number 5 Ocular pigmentation in cat 485
on the other hand, results from the failure of amese, such as a defective enzyme tyrosi-
neural crest-derived pigment cells to sur- nase, and that reduced pigmentation is mere-
vive.16' 32 Thus one finds amelanotic melano- ly one particular reflection of that defect.6
cytes, or "clear cells," in the skin and hair We are grateful to Miss W. Hughes who prepared the
bulbs of albino individuals but not in piebald histological slides. Mrs. E. van de Pol rendered valuable
individuals.16- 32- M technical assistance. We appreciated the technical sup-
Our observation of clear cells in the iris port provided by Messrs. L. M. Davies, R. M. Tupper,
stroma of the Siamese but not in the white cat and P. C. Kent and members of the Photographic Ser-
vice. The fundus camera used in this study was gen-
provides further experimental support for the erously provided by the Lions Club of Canberra.
idea that Siamese is a member of the albino
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