Download Ocular pigmentation in white and Siamese cats.

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
which have a deficiency of coat pigmentation
and which can also have reduced ocular pigmentation. The comparative details of this
hypopigmentation are of interest because the
Siamese cat suffers from an abnormal visual
pathway 1 " 3 yet the white cat does not. 4 Albino individuals of other mammalian species
have pathway abnormalities similar to those
in the Siamese cat, and the suggestion has
been made that the cause might be specifically related to the amount of pigment in the
retinal epithelium. 5 ' 6
From the Department of Physiology, John Curtin School
of Medical Research, Australian National University,
Canberra, Australia.
L. N. Thibos was supported by a Postdoctoral Fellowship of the U. S. Public Health Service. R. Morstyn
was a Vacation Scholar of the Australian National University.
Submitted for publication Dec. 27, 1978.
Reprint requests: Dr. W. R. Levick, Department of
Physiology, John Curtin School of Medical Research,
Australian National University, P.O. Box 334, Canberra City, A.C.T. 2601, Australia.
This report describes the extent of ocular
pigmentation in white cats as compared with
Siamese and normally pigmented cats. Several of the animals used in these experiments
were also subjects in neurophysiological investigations of the visual pathways which are
described elsewhere. 4
Methods
Ophthalmoscopic observations of six adult white
cats (A through F) of undetermined genetic constitution were made after each animal was prepared for neurophysiological recordings. The
pupil was dilated with atropine drops (1%), and a
zero-power contact lens was fitted. Additional observations were made on six white, five Siamese,
and one solid black cat (cats G through S). Color
photographs of the fundus and iris were taken with
a Zeiss fundus camera and Kodacolor 400 film.
Upon completion of neurophysiological experiments, a dose of about 30 mg of pentobarbitone
per kilogram of body weight was administered intravenously, and the eyes were enucleated. Each
eye was then hemisected at the pars plana, the
vitreous and lens were discarded, and the remainder was fixed in 10% neutral buffered formal
saline.
0146-0404/80/050475+12$01.20/0 © 1980 Assoc. for Res. in Vis. and Ophthal., Inc.
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476 Thibos, Levick, and Morstyn
Fig. 1. For legend see facing page.
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Invest. Ophthalmol, Vis. Set.
May 1980
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To get satisfactory iris preparations, animals G
through R, which were not part of neurophysiological experiments, were given 2 drops of 0.5%
physostigmine to contract the pupil. A lethal dose
of pentobarbitone was administered, and the eyes
were enucleated and fixed as described above.
Before the histological preparation was begun,
fundus tissue was sandwiched between slices of
fixed cat liver to minimize detachment of the retina from the choroid. Tissues were embedded in
paraffin, and 5 /u,m sections were prepared with
hematoxylin and eosin stain. In some preparations
melanin pigment was bleached by treatment with
0.1% potassium permanganate followed by 1%
oxalic acid. Photomicrographs were taken with a
Zeiss photomicroscope.
Results
Ophthalmoscopic and microdissection observations. A summary of the gross appearance of the irides and fundi of the 18 subjects
is given in Table I.
Iris. Color photographs of the living cat iris
are given in Fig. 1, A, for a yellow-eyed
white cat and in Fig. 1, C, for a blue-eyed
white cat. Dissection of the eyes of white cats
revealed the posterior surfaces of the irides to
be as darkly pigmented as in the ordinary
pigmented cat. Side-by-side comparison under transillumination showed that the yellow
and blue irides of white cats were each as
opaque as the yellow iris of a black cat.
The blue iris of a seal-point Siamese cat is
shown in Fig. 1, E. The posterior surface of
the Siamese iris was not as heavily pigmented
as in the ordinary pigmented cat, appearing a
dark chocolate brown in the seal point and a
lighter brown in the lilac point. Under trans-
Ocular pigmentation in cat
All
illumination the iris had a translucent to diaphanous appearance, quite different in sideby-side comparison with irides of white cats.
Fundus. The dominant feature of an ordinary pigmented cat's fundus is the yellowgreen tapetum which is surrounded by very
dark pigmentation. Although the precise size
and shape of the tapetum varies somewhat
from cat to cat,7 it is possible to predict the
location of the tapetum with acceptable reliability. We shall refer to this fiducial region
where one expects to find a tapetal reflection
as the tapetal zone. The statements which
follow are based upon complete ophthalmoscopic and microdissection surveys of the
entire fundi supported by selected fundus
photographs.
The fundi of yellow-eyed white cats had
the same appearance as those of ordinary
pigmented cats. A yellow-green reflection
from the tapetal zone and the retinal blood
vessels within this region were clearly visible
ophthalmoscopically (e.g., upper part of Fig.
1, B). The shape and size of the tapetum was
within the normal range.7 The nontapetal
zone appeared dark brown (e.g., lower part
of Fig. 1, B) due to the presence of pigment
in both the retinal epithelium and choroid as
observed by microdissection. However, in
eight of 12 eyes there were horizontally elongated patches of inferior fundus about 5 to
10 mm wide and 2 to 4 mm high where
choroidal pigment was completely missing.
Apart from these patches, the choroid was
equally heavily pigmented inside and outside
the tapetal zone.
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
Table I. Summary of macroscopic appearance of ocular pigmentation
Cat identification /breed
Eye
G
Bl
A
W
F
W
Y
Iris color
Iris epithelium
Choroid
Tapetum
Retina epithelium
outside tapetal
zone
H
W
R
L
R
L
R
L
R
L
Y
Y
Q
w
Y
D
W
E
W
L
W
C
W
w- w
R
W
SS
By
Y
By
Y
Bv
B
B
B
B
B
B
Y
I
J
B
W
p
B
N
SS
SS
K
LS
B
B
B
B
B
B
B
o
0
o
o 0 o
o o o
o
o
o
o
o
B
o
o
o
o
o
o
o
o
O
G
O
O
O
O
O
O
O
O
B
0
Of
O
o
o
o
o
o
o
o
o
o
o
R
s
M
SS
B
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
ordinary pigmented cat.8- 9 There was no
bright yellow reflection from the tapetal
zone, nor was there any choroidal pigmentation. Hence in vivo the tapetal zone had the
appearance of a jungle of red blood vessels
(e.g., upper part of Fig. 1, D). Microdissection of the fixed eyecup showed complete
lack of choroidal pigmentation. There were
the following exceptions. In three eyes a predominantly blue iris was partly yellow; in two
of these eyes the fundus had both tapetum
and choroidal pigment. In all the blue-eyed
white cats the pigment of the retinal epithelium was present outside the tapetal zone but
not within, just as in normal eyes. Pigmentation is shown in the lower part of Fig. 1, D,
partly obscuring the choroidal blood vessels.
The Siamese fundus in vivo showed a
slightly desaturated tapetal reflection (e.g.,
upper half of Fig. 1, F) and outside the
tapetal zone appeared reddish brown10 (e.g.,
lower part of Fig. 1, F). Microdissection
showed that there was no choroidal pigmentation. Visibility of the tapetum was reduced
in the fixed eye cup, probably because the
absence of choroidal pigment led to increased
amounts of scattered light. The distribution
of pigment in the retinal epithelium was the
same as for the white cats described above.
However, side-by-side comparison between
fundi of the Siamese and blue-eyed white
cats, neither of which had choroidal pigment,
showed that the white cat's epithelial pigment was significantly darker. Even at the
border of the tapetal zone where the epithelial pigmentation just began, it was observed
that the pigment clumps in the white cat
were darker than pigment in any part of the
Siamese retinal epithelium. This dilution of
epithelial pigment was quite definite in the
seal-point Siamese and even more obvious in
the lilac-point.
Histological observations
Yellow iris. A cross-sectional view of the
yellow iris taken from a black cat is shown in
Fig. 2, A, and from a yellow-eyed white cat in
Fig. 2, B. The pigmentation of the white cat's
iris is the same as for the black cat's iris: both
have heavily pigmented epithelial cells plus
light brown pigment cells of the stroma. The
stromal pigment is in the form of long thin
filaments similar to that found in rhesus monkey iris stromal cells11 known to be true melanocytes.12' 13 Thus it is likely that the cat's
stromal pigment cells are also melanocytes.
A magnified view of individual stromal
pigment cells is given in Fig. 3, A. Perikaryal
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Ocular pigmentation in cat
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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Invest. Ophthalmol. Vis. Set.
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Thibos, Levick, and Morstyn
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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Ocular pigmentation in cat
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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Invest, Ophthalmol. Vis. Set.
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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shape varies from nearly circular to long and
slender. A constant feature of these cells is
the large, darkly stained, oval nucleus. The
mean of the minimum and maximum nuclear
diameters determined for 20 cells ranged
from 4.75 to 7.25 /am and averaged 5.5 /xm.
Such nuclei were found only within the pigmented cells of the stroma.
Stromal pigment cells tended to be concentrated on the anterior surface of the iris. A
tangential section made parallel to the iris
surface therefore revealed a large number of
pigment cells for both black and yellow-eyed
white cats (Fig. 3, B). The greatest density of
pigment cells was found at invaginations and
at the margin of these sections, which was the
most anterior portion of the tissue.
Blue iris. Cross-sections of the blue-eyed
white cat's iris showed a normal, heavily
pigmented epithelium (Fig. 2, C). No pigmented cells were found in tangential sections of iris (Fig. 3, C). We ruled out the
possibility that such cells were present but
unpigmented, as suggested by Lauber,14 because none of the stromal nuclei had the
quantitative characteristics described above.
Pigmentation in the Siamese blue iris was
distinctly different from that of the blue-eyed
white cat. The layer of pigment within the
epithelium was thinner, and the granules
were less densely packed, particularly in the
lilac-point animal. Consequently individual
pigment granules could be observed, and
the normal pupillary ruff was hardly evident
(Fig. 2, D). The stroma was not pigmented,
but contrary to the situation in the blue-eyed
white cat, the pigment cells were evidently
present. This conclusion is based on the
tangential section of Fig. 3, D, which shows
many large oval nuclei having the expected
quantitative characteristics.
Fundus of the yellow eye. The comparison
of pigmentation in different eyes is most
straightforward if one avoids the margin of
the tapetal zone where the thickness of epithelial pigment varies. Accordingly, the data
presented below for the tapetal zone are from
the region about 3 mm above the area centralis and for the nontapetal zone is from the
Ocular pigmentation in cat 483
region about 7 mm below the area centralis.
Pigmentation of choroid and retinal epithelium in the nontapetal zone for a black cat
is shown in Fig. 4, A, and the yellow-eyed
white cat in Fig. 4, B. Epithelial pigment
thickness was in the range of 10 to 20 /Am in
these cats. A heavy infiltration of pigment
obscured the nuclei of the choroidal cells, but
bleaching revealed the nuclei to be of variable size and shape with no unambiguous
identifying characteristics. The thickness of
the choroid was due mainly to blood vessels
rather than the thin pigment cells.
Within the tapetal zone of the black (Fig.
5, A) and yellow-eyed white (Fig. 5, B) cat
fundus the retinal epithelium was devoid of
pigment, and the large, roughly circular nuclei of this single-cell layer were evident. The
tapetal cells were easily recognized by their
large nuclei, elongated perikaryon, regular
array, and particular coloration. The choroid
was equally heavily pigmented in the tapetal
and nontapetal zones.
Fundus of the blue eye. Outside the tapetal
zone the blue-eyed white cat's fundus (Fig.
4, C) had heavily pigmented retinal epithelial
cells. Above the area centralis within the
tapetal zone the retinal epithelium was unpigmented (Fig. 5, C) as in the ordinary pigmented cat, but tapetal cells were absent entirely. There was no choroidal pigmentation.
Because no unique features of choroidal pigment cells had been found in the ordinary
pigmented cat, we were unable to determine
whether in the blue-eyed white cat the pigment cells were present and unpigmented or
completely absent.
The Siamese cat had a thinner than normal
layer of pigment in the retinal epithelium in
the nontapetal zone (Fig. 4, D). From the
edge of the tape turn to the ora terminalis, the
maximum thickness of the epithelial pigment
layer in the seal-point retina was 5 (xm and in
the lilac-point 3 fxm, considerably less than in
the ordinary pigmented cat. Within the
tapetal zone there was no epithelial pigment
and the tapetal cells appeared normal. Choroidal pigmentation was completely absent
throughout the fundus, but it could not be
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Invest. Ophthalmol. Vis. Sci.
May 1980
484 Thibos, Levick, and Morstyn
determined whether the pigment cells were
absent altogether or present but devoid of
pigment.
Discussion
The results of this study are best summarized in relation to the postulated embryological source of the various types of ocular pigment cells. This is not known specifically for
the cat, but the following description is
common to other mammals,15' 16 birds,17 and
amphibia.18 Pigment cells of the iris and choroidal stromata are derived from cells which
migrate from the neural crest. The tapetal
cells of the cat are likely to be modified choroidal pigment cells19 and hence also of
neural crest origin. On the other hand, the
pigment epithelia of the retina and iris are
products of the embryonic eye cup.
Our results show that the yellow-eyed
white cat has normal ocular pigmentation but
the blue-eyed white cat lacks pigment in the
iridial and choroidal stromata. The basis of
the deficit in the blue eye appears to be the
absence of the pigment cell itself. Presumably the neural crest cells either failed to migrate to the ocular tissue or failed to differentiate and survive as uveal pigment cells.
The Siamese cat is also deficient in ocular
pigment but in quite a different way. First,
there is a relative diminution of pigmentation
of the iridial and retinal epithelia. Second,
the common lack of pigmentation in iridial
and choroidal stromata is associated with the
presence of unpigmented pigment cells, certainly in the iris and possibly also in the
choroid.
In summary, the blue-eyed white cat lacks
a particular cell type, whereas the Siamese is
defective in pigment production.
There were exceptions to the above generalizations. Three of 12 blue irides of white
cats had yellow sectors, and in one of these
eyes there was a patch of choroidal pigmentation. In eight of 12 yellow eyes of white
cats the choroidal pigmentation was incomplete. This heterogeneity might indicate the
presence of piebald spotting in the eye. It has
long been suspected20 that a blue eye would
appear if a cat carrying the gene for dominant
white also carried the gene pattern for
piebald spotting of the eye. White spots
would be undetectable in the completely
white hair and pink skin caused by dominant
white, but the edges of a spot might be revealed by the ocular pigment.
Tapetum lucidum. The results obtained
from blue-eyed white cats have shown that
the usual deletion of pigment from the retinal
epithelium within the tapetal zone is not
under direct tapetal control, since in these
cats the tapetal cells were absent but the distribution of retinal epithelial pigment was
normal.
Bernstein and Pease19 have suggested that
tapetal cells are modified choroidal melanocytes. The Siamese has heretofore been in
apparent contradiction to this hypothesis,
since choroidal pigment is missing yet the
animal has a normal tapetum. The inconsistency is resolved if the present results on iris
tissue are generalized to include choroid. We
may suppose that unpigmented choroidal
pigment cells are likely to be present in the
Siamese cat and therefore the derivative tapetal cells would be present as well. If this be
true, it would imply that functional tapetal
rods, which are the basis of light reflection
phenomena,21 are not dependent upon melanin production.
Genetics. The all-white coat of the white
cat is inherited as a dominant character8'20"22
and therefore cannot be the result of the action of an allele at the albino locus.23 There
has been only one report of an albino cat,24
but it is commonly believed that the Siamese
breed represents an imperfect form of albinism, as first suggested many years ago.25' 26
The evidence for this view is that (1) Siamese
is a recessive characteristic2' resulting in
hypopigmentation and (2) the pattern of
thermolabile coat pigmentation in the Siamese cat resembles that in the Himalayan
rabbit,28' 29 the gene of which is known to be
allelomorphic with the albino gene.27
The cause of the lack of pigment in albino
animals and some albino humans appear to
be a failure of individual melanocytes to produce pigment because of default of the enzyme tyrosinase.l6- 30> 31 A piebald white spot,
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on the other hand, results from the failure of
neural crest-derived pigment cells to survive.16' 32 Thus one finds amelanotic melanocytes, or "clear cells," in the skin and hair
bulbs of albino individuals but not in piebald
individuals.16- 32- M
Our observation of clear cells in the iris
stroma of the Siamese but not in the white cat
provides further experimental support for the
idea that Siamese is a member of the albino
series whereas dominant white is related to
piebaldism, and is consistent with the idea
first proposed by Wright34 that Siamese and
white cats are two breeds deficient in pigment as a result of entirely distinct genetic
mechanisms.
Optic nerve decussation. We have shown
elsewhere4 that the decussation of optic
nerve fibers in white cats is indistinguishable
from normal. Coupled with the present anatomical results, this means that normal development of the visual pathways may proceed without neural crest-derived pigment
cells and rules out the possibility that the
Siamese neural abnormality is simply due to
the lack of pigment in cells of neural crest
origin.
The hypothesis that neural development
depends upon optic cup pigmentation5-6 may
still be consistent with the results of this
paper. One argument against this view, however, is that in cats with normal visual pathways the retinal epithelium is unpigmented
in the tapetal zone. Examples from the literature7- 35 indicate that this unpigmented region is from V3 to V2 the area of the retina and
may include % of the retinal ganglion cells.36
If the adult pattern of epithelial pigment distribution is also present in the developing
embryo (an assumption we have verified in
fetuses as small as 11 mm crown-rump
length), then it is difficult to see how the
presence of pigmentation outside the tapetal
zone could control the decussation of axons
arising from ganglion cells within the tapetal
zone.
If the pigment hypothesis becomes untenable, then it may be that the embryonic control of optic nerve decussation is related to
some more fundamental abnormality in Si-
Ocular pigmentation in cat 485
amese, such as a defective enzyme tyrosinase, and that reduced pigmentation is merely one particular reflection of that defect.6
We are grateful to Miss W. Hughes who prepared the
histological slides. Mrs. E. van de Pol rendered valuable
technical assistance. We appreciated the technical support provided by Messrs. L. M. Davies, R. M. Tupper,
and P. C. Kent and members of the Photographic Service. The fundus camera used in this study was generously provided by the Lions Club of Canberra.
REFERENCES
1. Guillery RW: An abnormal retino-geniculate projection in Siamese cats. Brain Res 14:739, 1969.
2. Kalil R, Jhavery S, and Richards WR: Anomalous
retinal pathways in the Siamese cat: an inadequate
substrate for normal binocular vision. Science 174:
302, 1971.
3. Hubel DW and Wiesel TN: Aberrant visual projections in the Siamese cat. J Physiol 218:33, 1971.
4. Levick WR, Thibos LN, and Morstyn R: Retinal
ganglion cells and optic decussation in white cats.
(Submitted for publication.)
5. Sanderson KJ, Guillery RW, and Shackelford RM:
Congenitally abnormal visual pathways in mink
{hiustela vision) with reduced retinal pigment. J
Comp Neurol 154:225, 1974.
6. LaVail JR, Nixon RA, and Sidman RL: Genetic control of retinal ganglion cell projections. J Comp
Neurol 182:399, 1978.
7. Bishop PO, Kozak W, and Vakkur GJ: Some quantitative aspects of the cats eye: axis and plane of reference, visual field co-ordinates and optics. J Physiol 163:466, 1962.
8. Bergsma DR and Brown KS: White fur, blue eyes,
and deafness in the domestic cat. J Hered 62:171,
1971.
9. Tjebbes K: Crosses with Siamese cats. J Genet
14:355, 1924.
10. Johnson GL: Ophthalmoscopic studies on the eyes
of mammals. Philos Trans R Soc London Ser B
254:207, 1968.
11. Tousimis AJ: Pigment cells of the mammalian iris.
Ann NY Acad Sci 100:477, 1963.
12. Hu F and Montagna W: The development of pigment cells in the eyes of Rhesus monkeys. Am J
Anat 132:119, 1971.
13. Endo H and Hu F: Pigment cell development in
Rhesus monkey eyes: an electron microscopic and
histochemical study. Dev Biol 32:69, 1973.
14. Lauber H: Anatomische Untersuchungen iiber Heterochromie bei tauben, unvollkommen albinotischen Katzen. Ophthalmologica 16:326, 1908.
15. Rawles ME: Origin of pigment cells from the neural
crest in the mouse embryo. Physiol Zool 20:248,
1947.
16. Billingham RE and Silvers WK: The melanocytes of
mammals. Q Rev Biol 35:1, 1960.
Downloaded From: http://jov.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933322/ on 06/14/2017
486
Invest. Ophthalmol. Vis. Sci.
May 1980
Thibos, Levick, and Morstyn
17. Horstadius S: The Neural Crest. New York, 1950,
Oxford University Press.
18. Burden RB: The origin and development of the
chromatophores of the amphibian eye. J Exp Zool
90:479, 1942.
19. Bernstein MH and Pease DC: Electron microscopy
of the tape turn lucidum of the cat. J Biophys Biochem Cytol 5:35, 1959.
20. Whiting PW: Inheritance of coat color in cats. J Exp
Zool 25:539, 1918.
21. Coles JA: Some reflective properties of the tapetum
lucidum of the cat's eye. J Physiol 212:393, 1971.
22. Whiting PW: Inheritance of white-spotting and
other color characteristics in cats. Am Natur 53:473,
1919.
23. Witkop CJ, White JC, and King RA: Oculocutaneous albinism. In Heritable Disorders of Amino Acid
Metabolism: Patterns of Clinical Expression and
Genetic Variation, Nyhan WL, editor. New York,
1974, John Wiley & Sons, Inc., pp. 177-261.
24. Bamber RC and Herdman EC: Two new colourtypes in cats. Nature 127:558, 1931.
25. Bateson W: Mendel's Principles of Heredity.
Cambridge, England, 1909, Cambridge University
Press.
26. Castle WE: Siamese, an albinistic colour variation in
cats. Am Natur 53:265, 1919.
27. Keeler CE and Cobb V: Allelomorphism of silver
and Siamese coat variations in the domestic cat. J
Hered 24:181, 1933.
28. Schultz W: Willkiirliche Augenpigmentierung beim
Saugetieralbino. Arch Entwcklngsmechn Organismen 109:287, 1927.
29. Iljin NA and Iljin VN: Temperature effects on the
color of the Siamese cat. J Hered 21:309, 1930.
30. Fitzpatrick TB and Lerner AB: Biochemical basis of
human melanin pigmentation. Arch Dermatol
Syphilol 69:133, 1954.
31. Foster M: Mammalian pigment genetics. Adv Genet
13:311, 1965.
32. Silvers WK: Pigment cells: occurrence in hair follicles. J Morphol 99:41, 1956.
33. Becker SW, Fitzpatrick TB, and Montgomery H:
Human melanogenesis: cytology and histology of
pigment cells (melanodendrocytes). Arch Dermatol
Syphilol 65:511, 1952.
34. Wright S: Color inheritance in mammals. J Hered
9:139, 1918.
35. Hughes A: A supplement to the cat schematic eye.
Vision Res 16:149, 1976.
36. Hughes A: A quantitative analysis of the cat retinal
ganglion cell topography. J Comp Neurol 163:107,
1975.
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