Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T18:18:21.859Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  02 June 2009

Konrad Kohler ,
Walter Kolbinger ,
Gertrud Kurz-Isler  and
Reto Weiler
Konrad Kohler
Affiliation:
Department of Neurobiology, University of Oldenburg, Oldenburg, Federal Republic of Germany
Walter Kolbinger
Affiliation:
Department of Neurobiology, University of Oldenburg, Oldenburg, Federal Republic of Germany
Gertrud Kurz-Isler
Affiliation:
Department of Pathology, University of Tübingen, Tübingen, Federal Republic of Germany
Reto Weiler
Affiliation:
Department of Neurobiology, University of Oldenburg, Oldenburg, Federal Republic of Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

In the fish retina, retinomotor movement, spinule formation, and alteration of connexon density within gap junctions occur in response to changes in ambient light conditions. All of these morphological parameters can also be influenced by the application of dopamine. This study examines whether the morphological alterations of these structures are correlated with the activity of endogenous dopamine during an entrained 12-h light/12-h dark cycle and after 1-h sort-term adaptation periods.

The two measured parameters of retinomotor movement, cone inner segment length and pigment dispersion, were well-correlated with endogenous cyclic dopamine activity. However, retinomotor movement was initiated already at the end of the entrained dark period, before the onset of light and before the onset of dopamine turnover. Furthermore, a 1-h dark-adaptation period in the middle of the light phase reduced dopamine activity but did not affect retinomotor movement. At the switch from light to dark and after a 1-h light period at midnight retinomotor movement correlated exactly with dopamine turnover and illumination conditions. The formation of spinules was correlated with dopaminergic activity during all phases of the light/dark cycle and during short-term adaptation periods. Spinules were expressed in the light when dopamine activity was high and they were retracted when dopamine activity was reduced during darkness. Connexon density of horizontal cell gap junctions showed a weaker correlation with the endogenous dopamine turnover. In this case, a high activity of endogenous dopamine was paralleled by a high density of connexons.

Our results suggest that endogenous dopamine is involved in the cyclic regulation of the observed morphological alterations and that dopamine is part of the light signal for these mechanisms.

Keywords

RetinaEndogenous dopamineLight/dark cyclesRetinomotor movementHorizontal cells
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 5 , November 1990 , pp. 417 - 428
Copyright
Copyright © Cambridge University Press 1990

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. (1959). The ocular structure, retinomotor, and photobehavioral responses of juvenile pacific salmon. Canadian Journal of Zoology 37, 965–996.CrossRefGoogle Scholar
Ali, M.A. (1975). Retinomotor responses. In Vision in Fishes, ed. Ali, M.A., pp. 313–355. New York: Plenum Press.CrossRefGoogle Scholar
Arey, L.B. (1916). Movements in the visual cells and retinal pigment of the lower vertebrates. Journal of Comparative Neurology 26, 121–201.CrossRefGoogle Scholar
Baldridge, H.W., 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
Ball, A.K., Stell, W.K. & Tutton, D.A. (1989). Efferent projections to the goldfish retina. In Neurobiology of the Inner Retina, ed. Weiller, R. & Osborne, N., pp. 103–116. Heidelberg: Springer.CrossRefGoogle Scholar
Boatright, J.H., Hoel, M.J. & Iuvone, P.M. (1989). Stimulation of endogenous dopamine release and metabolism in amphibian retina by light and K+-evoked depolarization. Brain Research 482, 164–168.CrossRefGoogle ScholarPubMed
Brainard, G.C. & Morgan, W.W. (1987). Light-induced stimulation of retinal dopamine: a dose-response relationship. Brain Research 424, 199–203.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1985). Dopamine inhibits forskolin- and 3-isobutyl-1-methylxanthine-induced dark-adaptive retinomotor movement in isolated teleost retinas. Journal of Neurochemistry 44, 1753–1763.CrossRefGoogle ScholarPubMed
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, 1006–1022.CrossRefGoogle ScholarPubMed
Djamgoz, M.B.A., Downing, J.E.G., Kirsch, M., Prince, D.J. & Wagner, H.-J. (1988). Plasticity of cone horizontal cell functioning in cyprinid fish retina: effects of background illumination of moderate intensity. Journal of Neurocytology 17, 701–710.CrossRefGoogle ScholarPubMed
Douglas, R. & Wagner, H. (1982). Endogenous patterns of photomechanical movements and their relation to activity rhythms in teleost. Cell and Tissue Research 226, 133–142.CrossRefGoogle Scholar
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 201, 7–26.Google ScholarPubMed
Dowling, J.E. & Watling, K.J. (1981). Dopaminergic mechanisms in the teleost retina, II: Factors affecting the accumulation of cyclic AMP in pieces of intact carp retina. Journal of Neurochemistry 36, 567–579.CrossRefGoogle ScholarPubMed
Dubocovich, M.L., Lucas, R.C. & Takahashi, J.S. (1985). Light-dependent regulation of dopamine receptors in mammalian retina. Brain Research 335, 321–325.CrossRefGoogle ScholarPubMed
Fuortes, M.G.F. & Simon, E.J. (1974). Interactions leading to horizontal cell responses in the turtle retina. Journal of Physiology 240, 177–198.CrossRefGoogle ScholarPubMed
Iuvone, P.M., Galli, C.L., Garrison-Gund, C.K. & Neff, N.H. (1978). Light stimulates tyrosine hydroxylase activity and dopamine synthesis in retinal amacrine neurons. Science 202, 901–902.CrossRefGoogle ScholarPubMed
Iuvone, P.M. (1988). Dopamine: a light-adaptive modulator of melatonin synthesis in the frog retina. In Dopaminergic Mechanisms in Vision, ed. Bodis-Wollner, I. & Piccolino, M., pp. 95–107. New York: A.R. Liss.Google Scholar
John, K., Segall, M. & Zawatsky, L. (1967). Retinomotor rhythm in the goldfish (Carassius auratus). Biological Bulletin 132, 200–210.CrossRefGoogle ScholarPubMed
Kebabian, J. & Calne, D. (1979). Multiple receptors for dopamine. Nature 277, 93–96.CrossRefGoogle ScholarPubMed
Kolbinger, W., Kohler, K., Oetting, H. & Weiler, R. (1990). Endogenous dopamine and cyclic events in the fish retina, I: HPLC assay of total content, release, and metabolic turnover during different light/dark cycles. Visual Neuroscience 5, 143–159.CrossRefGoogle ScholarPubMed
Kurz-Isler, G. & Wolburg, H. (1986). Gap junctions between horizontal cells in the cyprinid fish alter rapidly their structure during light and dark adaptation. Neuroscience Letters 67, 7–12.CrossRefGoogle ScholarPubMed
Kurz-Isler, G. & Wolburg, H. (1988). Light-dependent dynamics of gap junctions between horizontal cells in the retina of the crucian carp. Cell and Tissue Research 251, 641–649.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, 7319–7323.CrossRefGoogle ScholarPubMed
Lasater, E.M. & Dowling, J.E. (1985). Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3025–3029.CrossRefGoogle ScholarPubMed
Mangel, S.L. & Dowling, J.E. (1985). Responsiveness and receptive-field size of carp horizontal cells are induced by prolonged darkness and dopamine. Science 229, 1107–1108.CrossRefGoogle Scholar
Parkinson, D. & Rando, R.R. (1983). Effects of light on dopamine metabolism in the chick retina. Journal of Neurochemistry 40, 39–46.CrossRefGoogle ScholarPubMed
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1984). Decrease of the gap-junction permeability induced by dopamine and cyclic 3–5 adenosine-monophosphate in horizontal cells of the turtle retina. Journal of Neuroscience 4, 2477–2488.CrossRefGoogle Scholar
Pierce, M.E. & Besharse, J.C. (1985). Circadian regulation of retinomotor movement, I: Interaction of melatonin and dopamine in the control of cone length. Journal of General Physiology 86, 671–689.CrossRefGoogle ScholarPubMed
Raynauld, J.-P., Laviolette, J.R. & Wagner, H.-J. (1979). Goldfish retina: a correlate between cone activity and morphology of the horizontal cell in cone pedules. Science 204, 1436–1438.CrossRefGoogle Scholar
Singh, I. (1964). A modification of the Masson-Hamperl method for staining of argentaffin cells. Anatomischer Anzeiger 115, 81–82.Google ScholarPubMed
Stell, W.K. & Lightfoot, D.O. (1975). Color specific interconnections of cones and horizontal cells in the retina of the goldfish. Journal of Comparative Neurology 159, 473–502.CrossRefGoogle ScholarPubMed
Stewart, W.W. (1981). Lucifer dyes – highly fluorescent dyes for biological tracing. Nature 292, 17–21.CrossRefGoogle ScholarPubMed
Studnitz, G. von (1933). Beiträge zur adaptation der teleosteer (studien zur vergleichenden physiologie der iris). Zeitschrift für vergleichende Physiologie 18, 307–338.CrossRefGoogle Scholar
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates Spotential amplitude and dye coupling between external horizontal cells in the carp retina. Nature 301, 243–246.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1984). Regulatory effect of dopamine on statial properties of horizontal cells in carp retina. Journal of Neuroscience 4, 1271–1280.CrossRefGoogle Scholar
Van Buskirk, R. & Dowling, J. (1981). Isolated horizontal cells from carp retina demonstrate dopamine-dependent accumulation of cyclic AMP. Proceedings of the National Academy of Sciences of the U.S.A. 78, 7825–7829.CrossRefGoogle ScholarPubMed
Wagner, H.-J. (1980). Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas. Journal of Neurocytology 9, 573–590.CrossRefGoogle ScholarPubMed
Watling, K.J. & Dowling, J.E. (1981). Dopaminergic mechanisms in the teleost retina, 1: Dopamine-sensitive adenylate cyclase in homogenates of carp retina: effects of agonists, antagonists, and ergots. Journal of Neurochemistry 36, 559–568.CrossRefGoogle ScholarPubMed
Weiler, R. & Wagner, H.-J. (1984). Light-dependent change of cone-horizontal cell interactions in carp retina. Brain Research 298, 1–9.CrossRefGoogle ScholarPubMed
Weiler, R., Kohler, K., Kirsch, M. & Wagner, H.-J. (1988 a). Glutamate and dopamine modulate synaptic plasticity in horizontal cell dendrites of fish retina. Neuroscience Letters 87, 205–209.Google ScholarPubMed
Weiler, R., Kohler, K., Kolbinger, W., Wolburg, H., Kurz-Isler, G. & Wagner, H.-J. (1988 b). Dopaminergic neuromodulation in the retinas of lower vertebrates. Neuroscience Research (Suppl.) 8, S183–S196.Google ScholarPubMed
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
Zucker, C.L. & Dowling, J.E. (1987). Centrifugal fibers synapse on dopaminergic interplexiform cells in the teleost retina. Nature 300, 166–168.CrossRefGoogle Scholar