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Solar pruning of retinal rods in albino rainbow trout

Published online by Cambridge University Press:  02 June 2009

Donald M. Allen  and
Ted E. Hallows
Donald M. Allen
Affiliation:
Department of Science and Mathematics, The University of Texas of the Permian Basin, Odessa
Ted E. Hallows
Affiliation:
Utah Division of Wildlife Resources, Kamas
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Abstract

Morphology of the central retina and scotopic visual sensitivity were compared in juvenile albino and normally pigmented rainbow trout living under natural and reduced daylight. Outdoor albinos avoided exposing their eyes to direct sunlight, whereas normals were indifferent to it. After 4 months outdoors (Σ10,000 lux in albinos, Σ100,000 lux in normals), albinos had severely truncated or missing rod outer segments (ROS) and some missing rod ellipsoids, but normal numbers of photoreceptor nuclei and fully intact cones. Albino estimated ROS volume was only 7.1% of normal in July, but increased to 20% by the following February, mainly via an increase in numbers of ROS. However, in albinos moved indoors October 7 and exposed to 10–30 lux ambient daylight, both the number and length of ROS increased significantly, with estimated ROS volume reaching 95% of normal by 34 days. Albinos generally had more phagosomes (Σ3 X normal) and more macrophages (Σ2 X normal) in their outer retina. An optomotor reflex was used to define the effect of ROS volume on the ability to respond visually during dark adaptation. In July, albinos and normals from outdoor raceways (3 months) or indoor raceways (35 days) showed equal sensitivity after first being placed in darkness, but after 1 h in darkness, outdoor albinos with 6% of normal ROS volume were 2.0 log units less sensitive than indoor or outdoor normals, whereas indoor albinos with 53% of normal ROS volume were only 0.7 log units less sensitive. This verifies that most rod cell bodies of albino trout can persist without functional ROS in indirect sunlight, and can regrow functional outer segments in dim daylight. This finding is distinct from the extensive retinal light damage observed in albino rats exposed to more moderate cyclic light, in which entire rod cells degenerate early on.

Keywords

RetinaPhotoreceptorsRetinal light damageVisual sensitivityAlbino trout
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 3 , May 1997 , pp. 589 - 600
Copyright
Copyright © Cambridge University Press 1997

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References

REFERENCES

Ali, M.A. (1964). Retina of the albino splake (Salvelinus fontinalis x S. namaycush). Canadian Journal of Zoology 42, 1158–1160.CrossRefGoogle Scholar
Ali, M.A. & Kobayashi, H. (1968 a). Electroretinogram—flicker fusion frequency in albino trout. Experientia 24, 454–455.CrossRefGoogle ScholarPubMed
Ali, M.A. & Kobayashi, H. (1968 b). Electroretinogram of albino and pigmented brook trout, Salvelinus fontinalis (Mitchell). Revue Canadienne Biology 2, 145–161.Google Scholar
Allen, D.M. (1995). Thermal control of rod outer segment length and shedding in a fish, Fundulus zebrinus. Experimental Eye Research 61, 165–171.CrossRefGoogle Scholar
Allen, D.M. & Munz, F.W. (1983). Visual pigment mixtures and scotopic visual sensitivity in rainbow trout. Environmental Biology of Fishes 8, 185–190.CrossRefGoogle Scholar
Allen, D.M. & Foreman, M. (1994). Shedding of rod photoreceptors after sunrise in fish. Experientia 50, 727–732.CrossRefGoogle Scholar
Anderson, R.E., Rapp, L.M. & Weigand, R.D. (1984). Lipid peroxidation and retinal degeneration. Current Eye Research 3, 223–227.CrossRefGoogle ScholarPubMed
Balkema, G.W. (1988). Elevated dark-adapted thresholds in albino rodents. Investigative Ophthalmology and Visual Science 29, 544–549.Google ScholarPubMed
Bassi, C.J. & Powers, M.K. (1990). Rod outer segment length and visual sensitivity. Investigative Ophthalmology and Visual Science 31, 2320–2325.Google ScholarPubMed
Bell, M.V., Batty, R.S., Dick, J.R., Fretwell, K., Navarro, J. & Sargent, J.R. (1995). Dietary deficiency of docosahexanoic acid impairs vision at low light intensities in juvenile herring (Clupea harengus, L.) Lipids 30, 443–449.CrossRefGoogle Scholar
Bell, M.V. & Tocher, D.R. (1989). Molecular species composition of the major phospholipids in brain and retina from rainbow trout (Salmo gairdneri). Biochemical Journal 264, 909–915.CrossRefGoogle ScholarPubMed
Bondari, K. (1984). Performance of albino and normal channel catfish (Ictalurus punctatus) in different water temperatures. Fisheries Management 15, 131–140.Google Scholar
Bridges, W.R. & Von Limbach, B. (1972). Inheritance of albinism in rainbow trout. Journal of Heredity 63, 152–153.Google Scholar
Burnside, B. & Nagle, B. (1983). Retinomotor movements of photoreceptors and retinal pigment epithelium: Mechanisms and regulation. Progress in Retinal Research 2, 67–108.Google Scholar
Bush, R. A., Reme, C.E. & Malnoe, A. (1991). Light damage in the rat retina: the effect of dietary deprivation of N-3 fatty acids on acute structural alterations. Experimental Eye Research 53, 741–752.Google Scholar
Cai, F. & Dickson, D.H. (1994). Diurnal change and prolonged dark effect on myeloid bodies in the retinal pigment epithelium of the leopard frog. Current Eye Research 13, 611–617.Google Scholar
Carter-Dawson, L., Kuwabara, T. & Bieri, J.G. (1981). Effects of moderate intensity light on vitamin A-deficient rat retinas. Investigative Ophthalmology and Visual Science 20, 569–574.Google Scholar
Chiu, J.F., Mack, A.F. & Fernald, R.D. (1995). Daily rhythm of cell proliferation in the teleost retina. Brain Research 673, 119–125.Google Scholar
Cicerone, C. (1976). Cones survive rods in the light-damaged eye of the albino rat. Science 194, 1183–1185.Google Scholar
Coggeshall, R.E. & Lekan, H.A. (1996). Methods for determining numbers of cells and synapses: A case for more uniform standards of review. Journal of Comparative Neurology 364, 6–15.Google Scholar
Cronly-Dillon, J.R. & Muntz, W.R.A. (1965). The spectral sensitivity of the goldfish and clawed toad under photopic conditions. Journal of Experimental Biology 42, 481–493.CrossRefGoogle ScholarPubMed
Cullen, A.P. & Monteith-Mcmaster, C.A. (1993). Damage to the rainbow trout (Oncorhyncus mykiss) lens following an acute dose of UVB. Current Eye Research 12, 97–106.Google Scholar
Delint, P.J., Van Norren, D. & Toebosch, A.M.W. (1992). Effect of body temperature on threshold for retinal light damage. Investigative Ophthalmology and Visual Science 33, 2382–2387.Google Scholar
Douglas, R.H. (1982). The function of photomechanical movements in the retina of the rainbow trout (Salmo gairdneri). Journal of Experimental Biology 96, 389–403.CrossRefGoogle Scholar
Douglas, R.H. (1983). Spectral sensitivity of rainbow trout (Salmo gairdneri). Revue Canadienne Biology Experimental 42, 117–122.Google Scholar
Dunn, M., Prasada, R. & Sharma, S. (1983). The ipsilateral retinotectal projection in abnormal and albino catfish. Neuroscience Letters (Ireland) 36, 25–31.Google Scholar
Dureau, P., Jeanny, J., Clerc, B., Dufier, J. & Courtois, Y. (1996). Long term light-induced degeneration in the miniature pig. Molecular Vision 2, 1–14.Google ScholarPubMed
Engbretson, G.A. & Witkovski, P. (1978). Rod visual sensitivity and visual pigment concentration in Xenopus. Journal of General Physiology 72, 801–819.CrossRefGoogle ScholarPubMed
Fliesler, S.J., Maude, M.B. & Anderson, R.E. (1983). Lipid composition of photoreceptor membranes from goldfish retinas. Biochemica and Biophysica Acta 734, 144–152.CrossRefGoogle Scholar
Gao, H. & Hollyfield, J.G. (1996). Basic fibroblast growth factor: Increased gene expression in inherited and light-induced photoreceptor degeneration. Experimental Eye Research 62, 181–189.CrossRefGoogle ScholarPubMed
Gordon, W.C. & Bazan, N.G. (1993). Visualization of [3H] Docosahexanoic acid trafficking through photoreceptors and retinal pigment epithelium by electron microscopic autoradiography. Investigative Ophthalmology and Visual Science 34, 2402–2411.Google Scholar
Grabowski, S.R. & Pak, W.L. (1975). Intracellular recording of responses during dark-adaptation. Journal of Physiology (London) 247, 363–391.Google Scholar
Green, D.G., De Tejada, P.H. & Glover, M.J. (1994). Electrophysiological estimates of visual sensitivity in albino and pigmented mice. Visual Neuroscience 11, 919–925.Google Scholar
Guillery, R.W. (1986). Neural abnormalities of albinos. Trends in Neuroscience 9, 364–367.Google Scholar
Hawryshyn, C.W., Arnold, M.G., Chaisson, D.J. & Martin, P.C. (1989). The ontogeny of ultraviolet photosensitivity in rainbow trout. Visual Neuroscience 2, 247–254.Google Scholar
Hayes, J.M. & Balkema, G.W. (1993). Visual thresholds in mice: Comparison of retinal light damage and hypopigmentation. Visual Neuroscience 10, 931–938.CrossRefGoogle ScholarPubMed
Hazel, J.R. (1995). Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation? Annual Review of Physiology 57, 19–42.CrossRefGoogle ScholarPubMed
Henton, W.W. & Sykes, S.M. (1983). Changes in absolute threshold with light-induced retinal damage. Physiology and Behavior 31, 179–185.CrossRefGoogle ScholarPubMed
Hitchcock, P.F. & Raymond, P.A. (1992). Retinal regeneration. Trends in Neuroscience 15, 103–108.Google Scholar
Jeffery, G. & Williams, A. (1994). Is abnormal retinal development in albinism only a mammalian problem? Normality of a hypopigmented avian retina. Expermental Brain Research 100, 47–57.Google Scholar
Jerlov, N.G. (1968). Optical Oceanography. Amsterdam: Elsevier.Google Scholar
Johns, P.R. (1977). Growth of the adult goldfish eye. III. Source of the new retinal cells. Journal of Comparative Neurology 176, 343–358.CrossRefGoogle ScholarPubMed
Johns, P.R. & Fernald, R.D. (1981). Genesis of rods in the retina of teleost fish. Nature 293, 141–142.Google Scholar
Julian, D. & Korenbrot, J.I. (1996). Cell proliferation in the mature inner nucler layer of the fish retina. Investigative Ophthalmology and Visual Science (ARVO Abstract) 37, S 692.Google Scholar
Kennedy, J.J. & Wood, D.B. (1977). Fisherman reaction to the stocking of albino rainbow trout in Utah. Progressive Fish Culturist 39, 16–17.Google Scholar
Lavail, M.M., Yasumura, D., Faktorovich, E.G., Hepler, I.M., Mattes, M.T., Pearson, K.L. & Steinberg, R. (1992). Basic fibroblast growth factor protects photoreceptors from light induced degeneration in albino rats. Annals NewYork Academy of Science 638, 1341–1347.Google Scholar
Mack, A.F. & Fernald, R. (1995). New rods move before differentiating in adult teleost retina. Developmental Biology 170, 136–141.Google Scholar
Mack, A.F., Balt, S.L. & Fernald, R.D. (1995). Localization and expression of insulin-like growth factor in the teleost retina. Visual Neuroscience 12, 457–461.Google Scholar
Marotte, L.R., Wye-Dvorak, J. & Mark, R.F. (1979). Retinotectal reorganization in goldfish—II. effects of partial tectal ablation and constant light on the retina. Neuroscience 4, 803–810.CrossRefGoogle ScholarPubMed
Matsuda, K., Watanabe, I., Unoki, K., Ohba, N. & Muramatsu, T. (1995). Functional rescue of photoreceptors from the damaging effects of constant light by survival-promoting factors in the rat. Investigative Ophthalmology and Visual Science 36, 2142–2146.Google Scholar
Mcfarland, W.N. (1986). Light in the sea—correlations with behaviors of fishes and invertebrates. American Zoologist 26, 389–401.Google Scholar
Mcfarland, W.N. & Allen, D.M. (1977). The effect of extrinsic factors on two distinctive rhodopsin-porphyropsin systems. Canadian Journal of Zoology 55, 1000–1009.Google Scholar
Noell, W.K. & Albrecht, R. (1971). Irreversible effects of visible light on the retina: Role of vitamin A. Science 172, 76–79.CrossRefGoogle ScholarPubMed
Noell, W.K., Walker, V.S., Kang, B.S. & Berman, S. (1966). Retinal damage by light in rats. Investigative Ophthalmology and Visual Science 5, 450–473.Google Scholar
Organisciak, D.T., Wang, H.M. & Noell, W.K. (1987). Aspects of the ascorbate protective mechanism in retinal light damage of rats with normal and reduced ROS docosahexanoic acid. In Degenerative Retinal Disorders, Clinical and Laboratory Investigations, ed. Hollyfield, J.G., Anderson, R.E. & Lavail, M.M., pp. 455–468. New York: Alan R. Liss, Inc.Google Scholar
Organisciak, D.T., Xie, A., Wang, H.-M., Jiang, Y.-L., Darrow, R.M. & Donoso, L.A. (1991). Adaptive changes in visual cell transduction protein levels: effect of light. Experimental Eye Research 53, 773–779.CrossRefGoogle ScholarPubMed
Organisciak, D.T. & Winkler, B.S. (1994). Retinal light damage: practical and theoretical considerations. Progress in Retinal Research 13, 1–29.Google Scholar
Page, J.W. & Andrews, J.W. (1975). Efects of light intensity and photoperiod on growth of normally pigmented and albino channel catfish. Progressive Fish Culturist 37, 121–122.CrossRefGoogle Scholar
Penn, J.S. (1985). Effects of continuous light on the retina of a fish, Notemigonus crysoleucas. Journal of Comparative Neurology 238, 2121–2127.Google Scholar
Penn, J.S. & Williams, T.P. (1986). Photostasis: regulation of daily photoncatch by rat retinas in response to various cyclic illuminances. Experimental Eye Research 43, 915–928.Google Scholar
Penn, J.S. & Anderson, R.E. (1991). Effects of light history on the rat retina. Progress in Retinal Research 11, 75–98.CrossRefGoogle Scholar
Powers, M.K. & Easter, S.S. (1978). Wavelength discrimination by the goldfish near absolute visual threshold. Vision Research 18, 1149–1154.Google Scholar
Prota, G. (1992). Melanins and Melanogenesis. San Diego, CA: Academic Press.Google ScholarPubMed
Rapp, L.M. & Williams, T.P. (1980). A parametric study of light damage in albino and pigmented rats. In Effects of Constant Light on Visual Processes, ed. Williams, T.P. & Baker, B.N., pp. 135–159. New York: Plenum Press.CrossRefGoogle Scholar
Rapp, L.M., Fisher, P.L. & Dhindsa, H.S. (1994). Reduced rate of rod outer segment disk synthesis in photoreceptor cells recovering from UVA light damage. Investigative Ophthalmology and Visual Science 35, 3540–3548.Google Scholar
Raymond, P.A., Bassi, C.J. & Powers, M.K. (1988). Lighting conditions and retinal development in goldfish: Photoreceptor number and structure. Investigative Ophthalmology and Visual Science 29, 27–36.Google Scholar
Raymond, P.A., Barrthel, L.K. & Rounsifer, M.E. (1992). Immunolocalization of basic fibroblast growth factor and its receptor in adult goldfish retina. Experimental Neurology 115, 73–78.CrossRefGoogle ScholarPubMed
Ripps, H. & Dowling, J.E. (1991). Structural features and adaptive properties of photoreceptors in the skate retina. Journal of Experimental Zoology (Suppl.) 5, 46–54.Google Scholar
Rothbard, S. & Wohlfarth, G.W. (1993). Inheritance of albinism in the grass carp, Ctenopharyngodon idella. Aquaculture 115, 13–17.Google Scholar
Sanyal, S. (1993). Synaptic growth in rod terminals after partial photoreceptor cell loss. Progress in Retinal Research 12, 247–270.Google Scholar
Sanyal, S., Deruiter, A. & Des, C. (1984). Light dependent accumulation of macrophages at the photoreceptor-pigment epithelial interface in the retina of albino mice. Experientia 40, 865–854.Google Scholar
Sarna, T. (1992). Properties and function of the ocular melanin—a photobiophysical view. Journal of Photochemistry and Photobiology B. Biology 12, 215–258.Google Scholar
Schmidt, K.-F., Billek, M., Pietruck, C., Noll, G.N., Goureau, O. & Courtois, Y. (1995). Fibroblast growth factors alter light responses and dark voltage in retinal rods of the frog (Rana temporaria). Neuroscience Letters 191, 177–180.Google Scholar
Schremser, J. & Williams, T.P. (1995). Rod outer segment (ROS) renewal as a mechanism for adaptation to a new intensity environment, II. Rhodopsin synthesis and packing density. Experimental Eye Research 61, 25–32.CrossRefGoogle ScholarPubMed
Semple-Rowland, S.L. & Dawson, W.W. (1987). Retinal cyclic light damage threshold for albino rats. Laboratory Animal Science 37, 289–298.Google Scholar
Shahinfar, S., Edward, D.E. & Tso, M.O.M. (1991). A pathologic study of photoreceptor cell death in retinal photic injury. Current Eye Research 10, 47–59.Google Scholar
Sokal, R.R. & Rholf, F.J. (1969). Biometry. San Francisco, California: W.H. Freeman & Co.Google Scholar
Spekreijse, H., Weitsma, J.J. & Neumeyer, C. (1991). Induced color blindness in goldfish: A behavioral and electrophysiological study. Vision Research 31, 551–562.Google Scholar
Thorgaard, G.H., Scheerer, P.D. & Zhang, J. (1992). Integration of chromosome set manipulation and transgenic technologies for fishes. Molecular Marine Biology Biotechnology 1, 251–256.Google Scholar
Tiku, P.E., Gracey, A.Y., Maccartney, A.I., Beynon, R.J. & Cossins, A.R. (1996). Cold-induced expression of δ9-desaturase in carp by transcriptional and posttranslational mechanisms. Science 271, 815–818.Google Scholar
Usukura, J., Khoo, W., Abe, T., Breitman, M. & Shinohara, T. (1994). Cone cells fail to develop normally in transgenic mice showing ablation of rod photoreceptor cells. Cell and Tissue Research 275, 79–90.Google Scholar
Wallaert, C. & Babin, P.J. (1994). Thermal adaptation affects the fatty acid composition of plasma phospholipids in trout. Lipids 29, 373–376.Google Scholar
Walls, G.L. (1942). The Vertebrate Eye and Its Adaptive Radiation. Bloom-field Hills, Michigan: Cranbrook Institute of Science.Google Scholar
Wang, G.L., Hull, B.E. & Organisciak, D.T. (1994). Long term effects of diaminophenoxypentane in the rat retina: Protection against light damage. Current Eye Research 13, 657–660.Google Scholar
Williams, T.P. & Howell, W.L. (1983). Action spectrum of retinal light damage in albino rats. Investigative Ophthalmology and Visual Science 24, 285–287.Google ScholarPubMed
Williams, R.A., Howard, A.G. & Williams, T.P. (1985). Retinal damage in pigmented and albino rats exposed to low levels of cyclic light following a single mydriatic treatment. Current Eye Research 4, 97–102.Google Scholar
Yamamoto, T. (1968). Inheritance of albinism in the medaka, Oryzias latipes, with special reference to gene interaction. Genetics 62, 797–809.Google Scholar
Yamamoto, T. (1973). Inheritance of albinism in the goldfish, Carassius auratus. Japanese Journal Genetics 48, 53–64.Google Scholar
Yorke, M.A. & Dickson, D.H. (1984). Diurnal variation in myeloid bodies of the newt retinal pigment epithelium. Cell and Tissue Research 235, 177–186.Google Scholar
Young, R.W. (1967). The renewal of photoreceptor outer segments. Journal of Cell Biology 33, 61–72.Google Scholar