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Depletion of retinal dopamine increases brightness perception in goldfish

Published online by Cambridge University Press:  02 June 2009

Zheng-Shi Lin
Affiliation:
Department of Neurobiology and Behavior, University at Stony Brook, Stony Brook
Stephen Yazulla
Affiliation:
Department of Neurobiology and Behavior, University at Stony Brook, Stony Brook

Abstract

The effect of unilateral depletion of retinal dopamine on goldfish visual behavior was studied using a behavioral reflex, the dorsal light reaction (DLR). Retinal dopamine was depleted by intraocular injections of 6–hydroxydopamine (6–OHDA) on two successive days. By 2 weeks postinjection, dopamine interplexiform cells (DA-IPC) were not detected using tyrosine-hydroxylase immunoreactivity (TH-IR). By 6 weeks postinjection, generation of DA-IPC was observed at the marginal zone and by 9 months postinjection, 2–3 rows of DA-IPC were present at the marginal zone. Neurites extended several hundred micrometers toward the central retina. By 2 weeks postinjection, all 6–OHDA lesioned fish tilted 7–15 deg toward the injected eye under uniform overhead illumination. The tilting did not occur under scotopic illumination and reappeared within 1 min of light adaptation. Quantitation of the DLR showed that 6–OHDA lesioned fish behaved as if light were 2.4 log units more intense to the injected eye. Partial recovery was observed by 9 months postinjection, paralleling the reappearance of DA-IPC at the marginal zone. Tilting also was induced by unilateral intraocular injection with Dl and D2 dopamine receptor antagonists, SCH 23390 and S(—)-sulpiride, respectively. Fish did not tilt if they were light adapted at the time of injection. Tilting was observed if the animals were dark-adapted for 3 h and left in the dark for 1 h postinjection. Fish tilted toward the drug-injected eye within 2 min of light adaptation and gradually returned to vertical within 2 h. The tilting response to S(—)-sulpiride was stronger (˜20 deg vs. ˜5 deg) and occurred at lower concentration (1 μM vs. 10 μM) compared to SCH 23390. We conclude that dopamine depletion mimics the dorsal light reaction by increasing the luminosity output of the eye and that dopamine is directly involved in photopic luminosity function.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

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References

Ali, M.A. (1975). Retinomotor responses. In Vision in Fishes, ed. Ali, M.A., pp. 313355. New York: Plenum Press.CrossRefGoogle Scholar
Baldridge, W.H., Ball, A.K. & Miller, R.G. (1987). Dopaminergic regulation of horizontal cell gap junction particle density in goldfish retina. Journal of Comparative Neurology 265, 428436.CrossRefGoogle ScholarPubMed
Baldridge, W.H. & Ball, A.K. (1991). Background illumination reduces horizontal cell receptive-field size in both normal and 6–hydroxydopamine-lesioned goldfish retinas. Visual Neuroscience 7, 441450.CrossRefGoogle ScholarPubMed
Ball, A.K., Baldridge, W.H. & Fernback, T.C. (1993). Neuro-modulation of pigment movement in the RPE of normal and 6–OHDA-lesioned goldfish retinas. Visual Neuroscience 10, 529540.CrossRefGoogle Scholar
Bodis-Wollner, I. (1990). Visual deficits related to dopamine deficiency in experimental animals and Parkinson's disease patients. Trends in Neuroscience 13, 296302.CrossRefGoogle ScholarPubMed
Bodis-Wollner, I. & Onofrj, M. (1984). The visual system in Parkinson's disease. Advances in Neurology 453, 323335.Google Scholar
Braisted, J.E. & Raymond, P.A. (1992). Regeneration of dopaminergic neurons in goldfish retina. Development 114, 913919.CrossRefGoogle ScholarPubMed
Buelow, N.F., Kelly, M.E. & Barlow, R.B. Jr. (1992). Dopamine: A circadian modulator of rod-cone dominance in quail? Investigative Ophthalmology and Visual Science (Suppl.) 33, 1406.Google Scholar
Cohen, J.L. & Dowling, J.E. (1983). The role of the retinal interplex-iform cell: Effects of 6–hydroxydopamine on the spatial properties of carp horizontal cells. Brain Research 264, 307310.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1985). Dopamine inhibits forskolin- and 3–isobutyl-l methylxanthine-induced dark-adaptive retinomotor movements in isolated teleost retinas. Journal of Neurochemistry 44, 17531763.CrossRefGoogle Scholar
Dearry, A. & Burnside, B. (1986). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: I. Induction of cone contraction is mediated by D2 receptors. Journal of Neurochemistry 46, 10061021.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1989). Light-induced dopamine release from teleost retinas acts as a light-adaptive signal to the retinal pigment epithelium. Journal of Neurochemistry 53, 870878.CrossRefGoogle Scholar
Djamgoz, M.B.A. & Wagner, H.-J. (1992). Invited review: Localization and function of dopamine in the adult vertebrate retina. Neurochemistry International 20, 139191.CrossRefGoogle Scholar
Douglas, R.H., Wagner, H.-J., Zaunreiter, M., Behrens, U.D. & Djamgoz, M.B.A. (1992). The effect of dopamine depletion on light-evoked and circadian retinomotor movements in the teleost retina. Visual Neuroscience 9, 335343.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Ehinger, B. (1978). The interplexiform cell system I. Synapses of the dopaminergic neurons of the goldfish retina. Proceedings of the Royal Society B (London) 201, 726.Google Scholar
Eldred, W.D., Zucker, C., Karten, H.J. & Yazulla, S. (1983). Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. Journal of Histochemistry and Cytochemistry 31, 285292.CrossRefGoogle ScholarPubMed
Ellis, C., Alen, T., Marsden, C. & Ikeda, H. (1987). Electromyographic abnormalities in idiopathic Parkinson's disease and the effect of levodopa administration. Clinical Visual Science 1, 347355.sGoogle Scholar
Ghilardi, M., Bodis-Wollner, I., Onofrj, M., Marx, M. & Glover, A. (1988 a). Spatial frequency-dependent abnormalities of the pattern electroretinogram and visual evoked potentials in a Parkinsonian monkey model. Brain 111, 131149.CrossRefGoogle Scholar
Ghilardi, M.F., Chung, E., Bodis-Wollner, I., Dvorzniak, M., Glover, A. & Onofrj, M. (1988 b). Systemic 1–methyl, 4–phenyl, 1–2–3–6–tetrahydropyridine (MPTP) administration decreases retinal dopamine content in primates. Life Sciences 43, 255262.CrossRefGoogle ScholarPubMed
Ghilardi, M., Marx, M., Bodis-Wollner, I., Camras, C. & Glover, A. (1989). The effect of intraocular 6–hydroxydopamine on retinal processing of primates. Annals of Neurology 25, 357364.CrossRefGoogle ScholarPubMed
Harsanyi, K. & Mangel, S.C. (1992). Activation of a D2 receptor increases electrical coupling between retinal horizontal cells by inhibiting dopamine release. Proceedings of the National Academy of Sciences of the U.S.A. 89, 92209224.CrossRefGoogle ScholarPubMed
Hedden, W.L. & Dowling, J.E. (1978). The interplexiform cell system II. Effects of dopamine on goldfish retinal neurones. Proceedings of the Royal Society B (London) 201, 2751.Google ScholarPubMed
Holst, E.V. (1935) Uber den lichtriickenreflex bei fishen. Pubblicazioni delta Stazione Zoologica di Napoli 15, 143158.Google Scholar
Wietsma, Jaap J. & Spekreuse, H. (1991). Bicuculline produces reversible red-green color blindness in goldfish, as revealed by monocular behavioral testing. Vision Research 31, 21012107.CrossRefGoogle ScholarPubMed
Knapp, A.G. & Dowling, J.E. (1987). Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 325, 437438.CrossRefGoogle ScholarPubMed
Kohler, K., Kolbinger, W., Kurz-Isler, G. & Weiler, R. (1990). Endogenous dopamine and cyclic events in the fish retina, II: Correlation of retinomotor movement, spinule formation, and connexon density of gap junctions with dopamine activity during light/dark cycles. Visual Neuroscience 5, 417428.CrossRefGoogle ScholarPubMed
Kurz-Isler, G. & Wolburo, H. (1986). Gap junctions between horizontal cells in the cyprinid fish alter rapidly their structure during light and dark adaptation. Neuroscience Letters 67, 712.CrossRefGoogle ScholarPubMed
Lasater, E.M. (1987). Retinal horizontal cell gap junctional conductance is modulated by dopamine through a cyclic AMP-dependent protein kinase. Proceedings of the National Academy of Sciences of the U.S.A. 84, 73197323.CrossRefGoogle ScholarPubMed
Malmfors, T. (1963). Evidence of adrenergic neurons with synaptic terminals in the retina of rats demonstrated with fluorescence and electron microscopy. Acta Physiologica Scandanavia 58, 99100.CrossRefGoogle ScholarPubMed
Mora-Ferrer, C. & Neumeyer, C. (1993). Reduced red-green discrimination in goldfish after application of dopamine antagonists. Investigative Ophthalmology and Visual Science (Suppl.) 34, 752.Google Scholar
Muller, E, Wassle, H. & Voigt, T. (1988). Pharmacological modulation of rod pathway in the cat retina. Journal of Neurophysiology 59, 16571672.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T. & Kato, S. (1982). New dopaminergic and indoleamine-accumulating cells in the growth zone of goldfish retinas after neurotoxic destruction. Science 216, 747749.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T., Kato, S. & Nakamura, Y. (1987). Paradoxical induction of dopaminergic cells following intravitreal injection of high doses of 6–hydroxydopamine in juvenile carp retina. Developmental Brain Research 33, 6779.CrossRefGoogle Scholar
Negishi, K., Teranishi, T. & Kato, K. (1990). The dopamine system of the teleost fish retina. Progress in Retinal Research 9, 148.CrossRefGoogle Scholar
Neumeyer, C. (1984). On spectral sensitivity in the goldfish. Evidence for neural interactions between different "cone mechanisms." Vision Research 24, 12231232.CrossRefGoogle ScholarPubMed
Neumeyer, C, Wietsma, J.J. & Spekreuse, H. (1991). Separate processing of "color" and "brightness" in goldfish. Vision Research 31, 537549.CrossRefGoogle Scholar
Northmore, D.P.M. & Yager, D. (1975). Psychophysical methods for investigations of vision in fishes. In Vision in Fishes, ed. Ali, M.A., pp. 689704. New York: Plenum.CrossRefGoogle Scholar
Pfeiffer, W. (1964). Equilibrium orientation in fish. In International Review of General Experimental Zoology, Vol. 1, ed. Felts, W.J.L. & Harrison, R.J., pp. 77111. New York: Academic Press.Google Scholar
Pierce, M.E. & Besharse, J.C. (1985). Circadian regulation of retinomotor movements: I. Interaction of melatonin and dopamine in the control of cone length. Journal of General Physiology 86, 671689.CrossRefGoogle ScholarPubMed
Powers, M.K. (1978). Light-adapted spectral sensitivity of the goldfish: A reflex measure. Vision Research 18, 11311136.CrossRefGoogle ScholarPubMed
Powers, M.K. & Easter, S.S. Jr. (1978). Absolute visual sensitivity of the goldfish. Vision Research 18, 11371148.CrossRefGoogle ScholarPubMed
Rashtd, K., Baidridge, W.H. & Ball, A.K. (1993) Evidence for D2 receptor regulation of dopamine release in the goldfish retina. Journal of Neurochemistry 61, 20252033.CrossRefGoogle Scholar
Schorderet, M. & Nowak, J.Z. (1990). Retinal dopamine D] and D2receptors: Characterization by binding or pharmacological studies and physiological functions. Cellular and Molecular Neurobiology 10, 303325.CrossRefGoogle ScholarPubMed
Silver, P.H. (1974). Photopic spectral sensitivity of the neon tetra (Paracheirodon innesi (Meyers)) found by the use of a dorsal light reaction. Vision Research 14, 329334.CrossRefGoogle Scholar
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 301, 243246.CrossRefGoogle ScholarPubMed
Umino, O., Lee, Y. & Dowling, J.E. (1991). Effects of light stimuli on the release of dopamine from interplexiform cells in the white perch retina. Visual Neuroscience 7, 451458.CrossRefGoogle ScholarPubMed
Van Haesendonck, E., Marc, R.E. & Missotten, L. (1993). New aspects of dopaminergic interplexiform cell organization in the goldfish retina. Journal of Comparative Neurology 333, 503518.CrossRefGoogle ScholarPubMed
Wagner, H.-J. & Behrens, U.D. (1993). Microanatomy of the dopaminergic system in the rainbow trout retina. Vision Research 33, 13451358.CrossRefGoogle ScholarPubMed
Wagner, H.-J. & Wulle, I. (1992). Contacts of dopaminergic interplexiform cells in the outer retina of the blue acara. Visual Neuroscience 9, 325333.CrossRefGoogle ScholarPubMed
Watling, K.J. & Dowling, J.E. (1981). Dopaminergic mechanisms in the teleost retina, I: Dopamine-sensitive adenylate cyclase in homog-enates of carp retina: Effects of agonists, antagonists, and ergots. Journal of Neurochemistry 36, 559568.CrossRefGoogle ScholarPubMed
Weiler, R., Kohler, K., Kirsch, M. & Wagner, H.-J. (1988). Glutamate and dopamine modulate synaptic plasticity in horizontal cell dendrites of fish retina. Neuroscience Letters 87, 205209.CrossRefGoogle ScholarPubMed
Witkovsky, P., Stone, S. & Tranchina, D. (1989). Photoreceptor to horizontal cell synaptic transfer in the Xenopus retina: Modulation by dopamine ligands and a circuit model for interactions of rod and cone inputs. Journal of Neurophysiology 62, 864881.CrossRefGoogle Scholar
Witkovsky, P. & Dearry, A. (1992). Functional roles of dopamine in the vertebrate retina. Progress Retinal Research 11, 113147.Google Scholar
Witkovsky, P. & Schütte, M. (1991). The organization of dopaminergic neurons in vertebrate retinas. Visual Neuroscience, 7 113124.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Shi, X.-P. (1990). Slow light and dark adaptation of horizontal cells in the Xenopus retina: A role for endogenous dopamine. Visual Neuroscience 5, 405413.CrossRefGoogle ScholarPubMed
Yazulla, S. (1985). Evoked efflux of 3H-GABA from goldfish retina in the dark. Brain Research 325, 171180.CrossRefGoogle ScholarPubMed
Yazulla, S. & Kleinschmidt, J. (1982). Dopamine blocks carrier mediated release of GABA from retinal horizontal cells. Brain Research 233, 211215.CrossRefGoogle ScholarPubMed