Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-26T01:15:38.084Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of dopamine depletion on light-evoked and circadian retinomotor movements in the teleost retina

Published online by Cambridge University Press:  02 June 2009

R. H. Douglas ,
H.-J. Wagner ,
M. Zaunreiter ,
U. D. Behrens  and
M. B. A. Djamgoz
R. H. Douglas
Affiliation:
Applied Vision Research Centre, Department of Optometry & Visual Science, City University, London, U.K.
H.-J. Wagner
Affiliation:
Institut für Anatomie und Zellbiologie der Phillips Universität, Marburg, Germany
M. Zaunreiter
Affiliation:
Institut für Anatomie und Zellbiologie der Phillips Universität, Marburg, Germany
U. D. Behrens
Affiliation:
Institut für Anatomie und Zellbiologie der Phillips Universität, Marburg, Germany
M. B. A. Djamgoz
Affiliation:
Department of Biology, Imperial College of Science, Technology and Medicine, niversity of London, U.K.
Get access Rights & Permissions [Opens in a new window]

Abstract

The retinae of lower vertebrates undergo a number of structural changes during light adaptation, including the photomechanical contraction of cone myoids and the dispersion of melanin granules within the epithelial pigment. Since the application of dopamine to dark-adapted retinae is known to produce morphological changes that are characteristic of light adaptation, dopamine is accepted as a causal mechanism for such retinomotor movements. However, we report here that in the teleost fish, Aequidens pulcher, the intraocular injection of 6-hydroxydopamine (6-OHDA), a substance known to destroy dopaminergic retinal cells, has no effect on the triggering of light-adaptive retinomotor movements of the cones and epithelial pigment and only slightly depresses the final level of light adaptation reached. Furthermore, the retina continues to show circadian retinomotor changes even after 48 h in continual darkness that are similar in both control and 6-OHDA injected fish. Biochemical assay and microscopic examination showed that 6-OHDA had destroyed dopaminergic retinal cells. We conclude, therefore, that although a dopaminergic mechanism is probably involved in the control of light-induced retinomotor movements, it cannot be the only control mechanism, nor can it be the cause of circadian retinomotor migrations. Interestingly, 6-OHDA injected eyes never reached full retinomotor dark adaptation, suggesting that dopamine has a role to play in the retina's response to darkness.

Keywords

RetinaDopamineTeleost6-HydroxydopamineEndogenous circadian rhythmPhotomechanicalRetinomotor
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 3-4 , October 1992 , pp. 335 - 343
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ali, M.A. (1975). Retinomotor responses. In Vision in Fishes: New Approaches in Research, ed Ali, M.A., pp. 313–356. New York: Plenum Press.CrossRefGoogle Scholar
Arey, L.B. & Mundt, G.H. (1941). A persistent diurnal rhythm in visual cones. Anatomical Record (Suppl.) 79, Abstract 41.Google 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, 428–436.CrossRefGoogle ScholarPubMed
Baldridge, W.H., Ball, A.K. & Miller, R.G. (1989). Gap junction particle density of horizontal cells in goldfish retinas lesioned with 6-OHDA. Journal of Comparative Neurology 287, 238–246.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, 441–450.CrossRefGoogle ScholarPubMed
Besharse, J.C. (1982). The daily light-dark cycle and rhythmic metabolism in the photoreceptor-pigment epithelium complex. Progress in Retinal Research 1, 81–124.CrossRefGoogle Scholar
Besharse, J.C., Iuvone, P.M. & Pierce, M.E. (1988). Regulation of rhythmic photoreceptor metabolism: A role for post-receptoral neurons. Progress in Retinal Research 7, 21–61.CrossRefGoogle Scholar
Bradford, H.F. (1986). Chemical Neurobiology. New York: Freeman.Google Scholar
Bruenner, U. & Burnside, B. (1986). Pigment granule migration in isolated cells of the teleost retinal pigment epithelium. Investigative Ophthalmology and Visual Science 27(11), 1634–1643.Google ScholarPubMed
Burnside, B. & Ackland, N. (1984). Effects of circadian rhythm and cAMP on retinomotor movements in the green sunfish, Lepomis cyanellus. Investigative Ophthalmology and Visual Science 25, 539–545.Google ScholarPubMed
Burnside, B. & Nagle, B. (1983). Retinomotor movements of photoreceptors and retinal pigment epithelium: Mechanisms and regulation. Progress in Retinal Research 2, 67–109.CrossRefGoogle Scholar
Burnside, B., Evans, M., Chader, G. & Fletcher, R.T. (1982). Induction of dark-adaptive retinomotor movement (cell elongation) in teleost retinal cones by cyclic adenosine 3′, 5′-monophosphate. Journal of General Physiology 79, 759–774.CrossRefGoogle ScholarPubMed
Dearry, A. (1991). Light onset stimulates tyrosine hydroxylase activity in isolated teleost retinas. Vision Research 31(3), 395–399.Google Scholar
Dearry, A. & Barlow, R.B. (1987). Circadian rhythms in the green sunfish retina. Journal of General Physiology 89, 745–770.Google Scholar
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, 1753–1763.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1986a). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: I. Induction of cone contraction is mediated by D2 receptors. Journal of Neurochemistry 46, 1006–1021.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1986b). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: I. Modulation by gamma-aminobutyric acid and serotonin. Journal of Neurochemistry 46, 1022–1031.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1988a). Dopamine induces light-adaptive retinomotor movements in teleost photoreceptors and retinal pigment epithelium. In Dopaminergic Mechanisms in Vision, ed Bodis-Wolner, I. & Piccolino, M., pp. 109–135. New York: Alan R. Liss, Inc.Google Scholar
Dearry, A. & Burnside, B. (1988b). Stimulation of distinct D2 dopaminergic and α2-adrenergic receptors induces light-adaptive pigment dispersion in teleost retinal pigment epithelium. Journal of Neurochemistry 51(5), 1516–1523.CrossRefGoogle Scholar
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, 870–878.Google Scholar
Dearry, A., Edelman, J.L., Miller, S. & Burnside, B. (1990). Dopamine induces light-adaptive retinomotor movements in bullfrog cones via D2 receptors and in retinal pigment epithelium via D1, receptors. Journal of Neurochemistry 54(4), 1367–1378.CrossRefGoogle ScholarPubMed
DeVries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. Journal of Physiology 414, 351–375.CrossRefGoogle ScholarPubMed
Djamgoz, M.B.A. & Wagner, H.-J. (1992). Localisation and function of dopamine in the adult vertebrate retina. Neurochemistry Internationally, 139–191.CrossRefGoogle ScholarPubMed
Douglas, R.H. (1982a). An endogenous crepuscular rhythm of rainbow trout (Salmo gairdneri) photomechanical movements. Journal of Experimental Biology 96, 377–388.Google Scholar
Douglas, R.H. (1982b). The function of photomechanical movements in the retina of the rainbow trout (Salmo gairdneri). Journal of Experimental Biology 96, 389–403.Google Scholar
Douglas, R.H. & Wagner, H.-J. (1982). Endogenous patterns of photomechanical movements in teleosts and their relation to activity rhythms. Cell and Tissue Research 226, 133–144.Google Scholar
Dowling, J.E. (1986). Dopamine: A retinal neuromodulator. Trends in Neuroscience 8, 236–240.CrossRefGoogle Scholar
Dowling, J.E. & Ehinger, B. (1978). The interplexiform cell system. Synapses of the dopaminergic neurons of goldfish retina. Proceedings of the Royal Society B (London) 201, 7–26.Google Scholar
Graham, W.C., Crossman, A.R. & Woodruff, G.N. (1990). Autoradiographic studies of animal models of hemi-parkinsonism reveal dopamine D2 but not D1, receptor supersensitivity. I. 6-OHDA lesions of ascending mesencephalic dopaminergic pathways in the rat. Brain Research 514, 93–102.CrossRefGoogle Scholar
Hamasaki, D.I., Trattler, W.B. & Hajek, A.S. (1986). Light on depresses and light off enhances the release of dopamine from the cat's retina. Neuroscience Letters 68, 112–116.CrossRefGoogle ScholarPubMed
Hida, E., Negishi, K. & Naka, K.-I. (1984). Effects of dopamine on photopic L-type S-potentials in the catfish retina. Journal of Neuroscience 11, 373–382.Google ScholarPubMed
John, K.R. & Haut, M. (1964). Retinomotor cycles and correlated behaviour in the teleost Astyanax mexicanus (Fillipi). Journal of the Fisheries Research Board of Canada 21, 591–595.CrossRefGoogle Scholar
John, K.R., Segall, M. & Zawatzky, L. (1967). Retinomotor rhythms in the goldfish, Carassius auratus. Biological Bulletin 132, 200–210.CrossRefGoogle ScholarPubMed
John, K.R. & Gring, D.M. (1968). Retinomotor rhythms in the bluegill, Lepomis macrochirus. Journal of the Fisheries Research Board of Canada 25, 373–381.Google Scholar
John, K.R. & Kaminester, L.H. (1969). Further studies on retinomotor rhythms in the teleost Astyanax mexicanus. Physiological Zoology 42, 60–70.CrossRefGoogle Scholar
Kirsch, M. & Wagner, H.-J. (1989). Release pattern of endogenous dopamine in teleost retinae during light adaptation and pharmacological stimulation. Vision Research 29, 147–154.CrossRefGoogle ScholarPubMed
Kirsch, M., Wagner, H.-J. & Djamgoz, M.B.A. (1991). Dopamine and plasticity of horizontal cell function in the teleost retina: Regulation of a spectral mechanism through D1 receptors. Vision Research 31, 401–412.CrossRefGoogle ScholarPubMed
Knapp, A.G. & Dowling, J.E. (1987). Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature (London) 325, 437–439.Google Scholar
Kohler, K. & Weiler, R. (1990). Dopaminergic modulation of transient neurite outgrowth from horizontal cells of the fish retina is not mediated by cAMP. European Journal of Neuroscience 2, 788–794.CrossRefGoogle Scholar
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, 417–428.CrossRefGoogle ScholarPubMed
Kolbinger, W., Kohler, K., Oetting, H. & Werer, R. (1990). Endogenous dopamine and cyclic events in the fish retina, I: HPLC assay of total content, and metabolic turnover during different light/dark cycles. Visual Neuroscience 5, 143–159.Google Scholar
Lasater, E.M. & Dowling, J.E. (1985). Dopamine decreases conductance of electrical junctions between cultured retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3025–3029.CrossRefGoogle ScholarPubMed
Levinson, G. & Burnside, B. (1981). Orcadian rhythms in teleost retinomotor movements: A comparison of the effects of circadian rhythm and light condition on cone length. Investigative Ophthalmology and Visual Science 20, 294–303.Google Scholar
Lythgoe, J.N. & Shand, J. (1983). Endogenous circadian retinomotor movements in the neon tetra (Paracheirodon innesi). Investigative Ophthalmology and Visual Science 24, 1203–1210.Google ScholarPubMed
Mangel, S.C. & Dowling, J.E. (1985). Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 229, 1107–1109.Google Scholar
Mangel, S.C. & Dowling, J.E. (1987). The interplexiform-horizontal cell system of the fish retina: Effects of dopamine, light stimulation and time in dark. Proceedings of the Royal Society B (London) 231, 91–121.Google Scholar
McCormack, C.A. & Burnside, B. (1991). Dopamine modulates circadian cone myoid movements in teleost retina. Investigative Ophthalmology and Visual Science 32(4), 847.Google Scholar
McMahon, D.G., Knapp, A.G. & Dowling, J.E. (1989). Horizontal cell gap junctions; single cell conductance and modulation by dopamine. Proceedings of the National Academy of Sciences of the U.S.A. 86(19), 7639–7643.Google Scholar
Muntz, W.R.A. & Richard, D.S. (1982). Photomechanical movements in the trout retina following brief flashes of light. Vision Research 22, 529–530.Google Scholar
Negishi, K. & Drujan, B.D. (1978). Effects of catecholamines on the horizontal cell membrane potential in the fish retina. Sensory Processes 2, 388–395.Google ScholarPubMed
Negishi, K. & Drujan, B.D. (1979). Effects of catecholamines and related compounds on horizontal cells in the fish retina. Journal of Neuroscience Research 4, 311–334.Google Scholar
Negishi, K., Teranishi, T. & Kato, S. (1982). Neurotoxic destruction of dopaminergic cells in the carp retina revealed by a histofluorescence study. Ada Histochemica and Cytochemica 15, 768–778.CrossRefGoogle Scholar
Negishi, K., Teranishi, T. & Kato, S. (1983). A GABA antagonist, bicuculline, exerts its uncoupling action on external horizontal cells through dopamine cells in carp retina. Neuroscience Letters 37, 261–266.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, 67–79.Google Scholar
Olla, B.L. & Marchioni, W.W. (1968). Rhythmic movements of cones in the retina of bluefish, Pomatomus saltatrix, held in constant darkness. Biological Bulletin 135, 530–536.CrossRefGoogle Scholar
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1984). Decrease of gap junction permeability induced by dopamine and cyclic adenosine 3′, 5′-monophosphate in the horizontal cells of turtle retina. Journal of Neuroscience 4, 2477–2488.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, 671–689.Google Scholar
Richardson, K.C., Jarett, L. & Finke, E.H. (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technology 35, 313–323.CrossRefGoogle ScholarPubMed
Rogawski, M.A. (1987). New directions in neurotransmitter action: Dopamine provides some important clues. Trends in Neuroscience 10(5), 200–205.CrossRefGoogle Scholar
Shigematsu, Y. & Yamada, M. (1988). Effects of dopamine on spatial properties of horizontal cell responses in the carp retina. Neuroscience Research (Suppl.) 8, 69–80.Google Scholar
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature (London) 301, 243–246.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1984). Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina. Journal of Neuroscience 4, 1271–1280.CrossRefGoogle ScholarPubMed
Tornqvist, K., Yang, X.-L. & Dowling, J.E. (1988). Modulation of cone horizontal cell activity in the teleost fish retina. III. Effects of prolonged darkness and dopamine on electrical coupling between horizontal cells. Journal of Neuroscience 8, 2279–2288.Google Scholar
Wagner, H.-J. & Douglas, R.H. (1983). Morphologic changes in teleost primary and secondary retinal cells following brief exposure to light. Investigative Ophthalmology and Visual Science 24, 24–29.Google Scholar
Wagner, H.-J. & Wulle, I. (1990). Dopaminergic interplexiform cells contact photoreceptor terminals in catfish retina. Cell and Tissue Research 261, 359–365.CrossRefGoogle Scholar
Wagner, H.-J., Behrens, U.D., Zaunreiter, M. & Douglas, R.H. (1992). The circadian component of spinule dynamics in teleost retinal horizontal cells is dependent on the dopaminergic system. Visual Neuroscience 9, 345–351.CrossRefGoogle ScholarPubMed
Weiler, R., Kohler, K., Kirsch, M. & Wagner, H.-J. (1988a). Glutamate and dopamine modulate synaptic plasticity in horizontal cell dendrites of fish retina. Neuroscience Letters 87, 205–209.Google Scholar
Weiler, R., Kohler, K., Kolbringer, W., Wolburg, H., Kurz-Isler, G. & Wagner, H.-J. (1988b). Dopaminergic neuromodulation in the retina of lower vertebrates. Neuroscience Research (Suppl.) 8, 183–196.Google Scholar
Weiler, R., Kolbinger, W. & Kohler, K. (1989). Reduced light responsiveness of the cone pathway during prolonged darkness does not result from an increase of dopaminergic activity in the fish retina. Neuroscience Letters 99, 214–218.CrossRefGoogle Scholar
Welsh, J.H. & Osborn, C.M. (1937). Diurnal changes in the retina of the catfish, Ameiurus nebulosus. Journal of Comparative Neurology 66, 349–359.Google Scholar
Witkovsky, P., Alones, V. & Piccolino, M. (1987). Morphological changes induced in turtle retinal neurons by exposure to 6-hydroxydopamine and 5, 6-dihydroxytryptamine. Journal of Neurocytology 16, 55–67.CrossRefGoogle ScholarPubMed
Wulle, I., Kirsch, M. & Wagner, H.-J. (1990). Cyclic changes in dopamine and DOPAC content, and tyrosine hydroxylase activity in the retina of a cichlid fish. Brain Research 515, 163–167.Google Scholar
Yang, X.-L., Tauchi, M. & Kaneko, A. (1988a). Convergence of signals from red-sensitive and green-sensitive cones onto L-type external horizontal cells of the goldfish retina. Vision Research 28, 371–380.Google Scholar
Yang, X.-L., Tornqvist, K. & Dowling, J.E. (1988b). Modulation of cone horizontal cell activity in the teleost fish retina. I. Effects of prolonged darkness and background illumination on light responsiveness. Journal of Neuroscience 8, 2258–2268.Google Scholar
Yazulla, S. & Zucker, C.L. (1988). Synaptic organization of dopaminergic interplexiform cells in the goldfish retina. Visual Neuroscience 1, 13–29.Google Scholar
Zigmond, M.J., Abercrombie, E.D., Berger, T.W., Grace, A.A. & Stricker, E.M. (1990). Compensation after lesions of central dopaminergic neurons: Some clinical and basic implications. Trends in Neuroscience 13, 290–296.Google Scholar