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Impaired visual thresholds in hypopigmented animals

Published online by Cambridge University Press:  02 June 2009

Grant W. Balkema  and
Ursula C. Dräger
Grant W. Balkema
Affiliation:
Department of Biology, Boston College, Chestnut Hill
Ursula C. Dräger
Affiliation:
Department of Neurobiology, Harvard Medical School, Boston
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Abstract

Ocular hypopigmentation is associated with neurological defects in structure and function. This paper investigates the ab/Fute visual thresholds in dark-adapted hypopigmented animals compared to their normally pigmented controls. Here we asked (1) whether the threshold elevation found in hypopigmented animals is a general consequence of the reduction in melanin content; (2) if so, which melanin components in the eye are likely to influence visual thresholds; and (3) whether similar threshold defects can be detected in orders other than rodents. By single-unit recordings from the superior colliculus, we compared incremental thresholds of normal black mice of the C57BL/6J strain to hypopigmented mutants: beige (bg/bg), pale ear (ep/ep), and albino (c2J/c2J) mice, three mutants in which melanin pigment throughout the body is affected; and Steel (Sl/Sld) and dorninant-spotting/W-mice (W/Wν), two mutants with normal pigmentation in the retinal pigment epithelium (RPE) but without any melanin in the choroid or the rest of the body. We found that all mutants had elevated thresholds that varied with the reduction in melanin. The albinos were 25 times less sensitive than black mice, pale ear mice 20 times, beige mice 11 times, and Steel and W-mice 5 times. The mean thresholds of dark-adapted black mice were 0.008 cd/m2. Recordings from rabbits showed a similar impairment of visual sensitivity: incremental thresholds were elevated 40 times in New Zealand-White albino rabbits (0.0008 cd/m2) compared to Dutch-Belted pigmented controls (0.00002 cd/m2). Previously, it has been shown that hypopigmented rats have elevated dark-adapted thresholds compared to pigmented controls (Balkema, 1988); here we show that the difference between hypopigmented rats and pigmented controls is not caused by insufficient dark adaptation or excessive variability in the results from albino mutant compared to its control.

Mutations that cause a reduction of ocular melanin pigmentation, regardless of the gene mutated or the mechanism underlying the hypopigmentation, are accompanied by an elevation in visual thresholds which is roughly proportional to the reduction in melanin. Melanin both in the RPE and choroid exert an effect on visual thresholds. Like the defects in optic nerve crossing and eye movements, the effect of melanin on visual thresholds is not restricted to rodents, but is seen in other orders. The threshold impairment in hypopigmented animals cannot be explained by impaired photoprotection, but it points to another physiological action of melanin.

Keywords

MelaninMouseRatRabbitAlbinoPearlBeigePale earsSteelNight blindness
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 6 , June 1991 , pp. 577 - 585
Copyright
Copyright © Cambridge University Press 1991

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References

Balkema, G.W. (1988). Elevated dark-adapted thresholds in albino rodents. Investigative Ophthalmology and Visual Science 29, 544–554.Google ScholarPubMed
Balkema, G.W. & Dräger, U.C. (1990). Origins of uncrossed retinofugal projections in normal and hypopigmented mice. Visual Neuroscience 4, 594–604.CrossRefGoogle ScholarPubMed
Balkema, G.W., Mangini, N.J. & Pinto, L.H. (1983). Discrete visual defects in pearl mutant mice. Science 219, 1085–1087.CrossRefGoogle ScholarPubMed
Balkema, G.W., Mangini, N.J., Pinto, L.H. & Vanable, J.W. Jr (1984). Visually evoked eye movements in mouse mutants and inbred strains. A screening report. Investigative Ophthalmology and Visual Science 25, 795–800.Google ScholarPubMed
Balkema, G.W. & Pinto, L.H. (1982). Electrophysiology of retinal ganglion cells in the mouse: a study of a normally pigmented mouse and a congenic hypopigmentation mutant, pearl. Journal of Neurophysiology 48, 968–980.CrossRefGoogle Scholar
Balkema, G.W., Pinto, L.H., Dräger, U.C. & Vanable, J.W. Jr (1981). Characterization of abnormalities in the visual system of the mutant mouse pearl. Journal of Neuroscience 1, 1320–1329.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1969). Three factors limiting the reliable detection of light by retinal ganglion cells of the cat. Journal of Physiology 200, 1–24.CrossRefGoogle ScholarPubMed
Bonaventure, N. & Karli, P. (1961). Sur la sensibilit? spectrale de l'appareil visuel chez la Souris. Comptes Rendus des Séances de la Société de Biologie 155, 455–456.Google Scholar
Cicerone, C.M. & Green, D.G. (1980). Light adaptation within the receptive-field center of rat retinal ganglion cells. Journal of Physiology 301, 517–534.CrossRefGoogle ScholarPubMed
Cone, R.A. (1963). Quantum relations of rat electroretinogram. Journal of General Physiology 46, 1267–1286.CrossRefGoogle ScholarPubMed
Creel, D.J. (1980). Inappropriate use of albino animals as models in research. Pharmacology, Biochemistry and Behavior, 12, 969–977.Google ScholarPubMed
Creel, D.J., Conlee, J.W. & King, R.A. (1990). Dark adaptation in human albinos. Clinical Vision Science 5, 81–85.Google Scholar
Creel, D.J. & Giolli, R.A. (1976). Retinogeniculate projections in albino and ocularly hypopigmented rats. Journal of Comparative Neurology 160, 269–290.Google Scholar
Dodt, E. & Echte, K. (1961). Dark and light adaptation in pigmented and white rat as measured by electroretinogram threshold. Journal of Neurophysiology 24, 427–445.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1963). Neural and photochemical mechanisms of visual adaptation in the rat. Journal of General Physiology 46, 1287–1301.CrossRefGoogle ScholarPubMed
Dräger, U.C. (1985 a). Birth dates of retinal ganglion cells giving rise to the crossed and uncrossed optic projections in the mouse. Proceedings of the Royal Society B (London) 224, 57–77.Google Scholar
Dräger, U.C. (1985 b). Calcium binding in pigmented and albino eyes. Proceedings of the National Academy of Sciences of the U.S.A. 82, 6716–6720.CrossRefGoogle ScholarPubMed
Dräger, U.C. & Balkema, G.W. (1987). Does melanin do more than protect from light? Neuroscience Research 38, S75–S86.Google Scholar
Dräger, U.C. & Hubel, D.H. (1978). Studies of visual function and its decay in mice with hereditary retinal degeneration. Journal of Comparative Neurology 180, 85–114.CrossRefGoogle ScholarPubMed
Dräger, U.C. & Hubel, D.H. (1975). Physiology of visual cells in mouse superior colliculus and correlation with somatosensory and auditory input. Nature 253, 203–204.CrossRefGoogle ScholarPubMed
Ebrey, T.G. & Cone, R.A. (1967). Melanin, a possible pigment for the photostable electrical responses of the eye. Nature 213, 360–362.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Pinto, L.H. (1972). Pure central responses from OFF-center cells and pure surround responses from ON-center cells. Journal of Physiology 220, 441–464.CrossRefGoogle Scholar
Fitzpatrick, T.B., Szabo, G. & Wick, M.M. (1983). Biochemistry and physiology of melanin pigmentation. In Biochemistry and Physiology of the Skin, ed. Oxford, G.L.A., New York: Oxford University Press.Google Scholar
Green, D.G. (1971). Light adaptation in the rat retina: evidence for two receptor mechanisms. Science 174, 598–600.CrossRefGoogle ScholarPubMed
Green, D.G. & Powers, M.K. (1982). Mechanisms of light adaptation in rat retina. Vision Research 22, 209–216.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1969). An abnormal retinogeniculate projection in Siamese cats. Brain Research 14, 739–741.CrossRefGoogle ScholarPubMed
HerrerosDe Tejada, P. De Tejada, P., Green, D.G. & Glover, M.J. (1990). Do albino rats have elevated dark-adapted thresholds? Investigative Ophthalmology and Visual Science 31, 391.Google Scholar
Hess, H.H. (1975). The high calcium content of retinal pigment epithelium. Experimental Eye Research 21, 471–479.CrossRefGoogle Scholar
Hood, J.D., Poole, J.P. & Freedman, L. (1976). Eye color and susceptibility to TTS. Journal of the Acoustical Society of America 59, 706–707.CrossRefGoogle ScholarPubMed
Hughes, A. (1971). Topographical relationships between the anatomy and physiology of the rabbit visual system. Documenta Ophthalmologica 30, 33–160.CrossRefGoogle ScholarPubMed
Larsson, B. (1979). Mechanisms of accumulation of foreign substances in melanin. Acta Universitatis Upsaliensis 43, 1–52.Google Scholar
LaVail, M., Gorrin, G.M., Repaci, M.A., Thomas, L.A. & Ginsberg, H.M. (1987). Genetic regulation of light damage to photoreceptors. Investigative Ophthalmology and Visual Science 28, 1043–1048.Google ScholarPubMed
LaVail, J.H., Nixon, R.A. & Sidman, R.L. (1978). Genetic control of retinal ganglion cell projections. Journal of Comparative Neurology 182, 399–421.CrossRefGoogle ScholarPubMed
Lindquist, N.G. (1973). Accumulation of drugs on melanin. Acta Radiologica (Suppl.) 325, 1–92.Google ScholarPubMed
Lund, R.D. (1965). Uncrossed visual pathways of hooded and albino rats. Science 149, 1506–1507.CrossRefGoogle ScholarPubMed
Mangini, N.J., Vanable, J.W. Jr, Williams, M.A. & Pinto, L.H. (1985). The optokinetic nystagmus and ocular pigmentation of hypopigmented mouse mutants. Journal of Comparative Neurology 241, 191–209.CrossRefGoogle ScholarPubMed
McFadden, D. & Wightman, F.L. (1983). Audition: some relations between normal and pathological hearing. Annual Review Psychology 34, 95–128.CrossRefGoogle ScholarPubMed
Pak, M.W., Giolli, R.A., Pinto, L.H., Mangini, N.J., Gregory, K.M. & Vanable, J.W. Jr (1987). Retino-pretectal and accessory optic projections of normal mice and the OKN-defective mutant mice beige, beige-J, and pearl. Journal of Comparative Neurology 258, 435–446.CrossRefGoogle Scholar
Pawelek, J.M. & Körner, A.M. (1982). The biosynthesis of mammalian melanin. American Scientist 70, 136–145.Google ScholarPubMed
Potts, A.M. & Au, P.C. (1976). The affinity of melanin for inorganic ions. Experimental Eye Research 22, 487–491.CrossRefGoogle ScholarPubMed
Powers, M.K. & Green, D.G. (1978). Single retinal ganglion cell responses in the dark-reared rat: grating acuity, contrast sensitivity, and defocusing. Vision Research 18, 1533–1539.CrossRefGoogle ScholarPubMed
Robinson, W.G., Kuwabara, T. & Cogan, D.G. (1975). Lysosomes and melanin granules of the retinal pigment epithelium in a mouse model of the Chediak-Higashi syndrome. Investigative Ophthalmology and Visual Science 14, 312–317.Google Scholar
Royster, L.H., Royster, J.D. & Thomas, W.G. (1980). Representative hearing levels by race and sex in North Carolina Industry. Journal of the Acoustical Society of America 68, 551–566.CrossRefGoogle ScholarPubMed
Sanderson, K.J., Guillery, R.W. & Shackelford, R.M. (1974). Congenitally abnormal visual pathways in mink (Mustela vision) with reduced retinal pigment. Journal of Comparative Neurology 154, 225–248.CrossRefGoogle ScholarPubMed
Sawin, P.B. & Glick, D. (1943). Atropinesterase, genetically determined enzymes in the rabbit. Proceedings of the National Academy of Sciences of the U.S.A. 29, 55–59.CrossRefGoogle ScholarPubMed
Sealy, R.C., Felix, C.C., Hyde, J.S. & Swartz, H.M. (1980). Structure and reactivity of melanins: influence of free radicals and metal ions. In Free Radicals in Biology. ed. Pryor, W.A., pp. 209–259. New York: Academic Press.CrossRefGoogle Scholar
Searle, A.G. (1968). Comparative Genetics of Coat Color in Mammals. London: Academic Press.Google Scholar
Shatz, C.J. & Kliot, M. (1982). Prenatal misrouting of the retino-geniculate pathway in Siamese cats. Nature 300, 525–529.CrossRefGoogle Scholar
Silvers, W.K. (1979). The Coat Colors of Mice. New York: Springer-Verlag.CrossRefGoogle Scholar
Suzuki, H. & Pinto, L.H. (1986). Response properties of horizontal cells in the isolated retina of wildtype and pearl mutant mice. Journal of Neuroscience 6, 1122–1128.CrossRefGoogle ScholarPubMed
Tota, G. & Bocci, G. (1967). L'importanza del colore dell'iride nella valutazione della resistenza dell'udito all'affaticamento. Rivista Oto-Neuro-Oftalmolgica (Bologna) 42, 183–192.Google Scholar
Wasterstrom, S.A., Bredberg, G., Lindquist, N.G. & Lyttkens, L. (1986). Ototoxicity of kanamycin in albino and pigmented guinea pigs. American Journal of Otology 7, 11–18.Google ScholarPubMed
Williams, M.A., Pinto, L.H. & Gehrson, J. (1985). The retinal pigment epithelium of wild-type (C57BL/6J +/+) and pearl mutant (C57BL/6J pe/pe) mice. Investigative Ophthalmology and Visual Science 26, 657–669.Google ScholarPubMed
Winterson, B.J. & Colledwijn, H. (1981). Inversion of direction selectivity to anterior fields in neurons of nucleus of the optic tract in rabbits with ocular albinism. Brain Research 220, 31–49.CrossRefGoogle ScholarPubMed