Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-25T05:57:04.327Z Has data issue: false hasContentIssue false
  • English
  • Français

The circadian component of spinule dynamics in teleost retinal horizontal cells is dependent on the dopaminergic system

Published online by Cambridge University Press:  02 June 2009

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

Abstract

During the light phase of a light/dark cycle, dendrites of teleost cone horizontal cells display numerous finger-like projections, called spinules, which are formed at dawn and degraded at dusk, and are thought to be involved in chromatic feedback processes. We have studied the oscillations of these spinules during a normal light/dark cycle and during 48 h of constant darkness in two groups of strongly rhythmic, diurnal fish, Aequidens pulcher. In one group the retinal dopaminergic system had been destroyed by the application of 6-OHDA, while in the other (control) group, the dopaminergic system was intact. In control fish, oscillations of spinule numbers were observed under both normal and constant dark conditions, indicating the presence of a robust circadian rhythm. However, spinule dynamics were severely affected by the absence of retinal dopamine. During the normal light phase, the number of spinules in 6-OHDA injected retinae was strongly reduced, and throughout continual darkness, spinule formation was almost completely suppressed. These results indicate that dopamine is essential for both light-evoked and circadian spinule formation; furthermore, we conclude that there is no circadian oscillator within horizontal cells controlling the formation of spinules.

Keywords

AdaptationDopamine6-HydroxydopamineEndogenous circadian rhythmSynaptic plasticity
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 3-4 , October 1992 , pp. 345 - 351
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. 313–355. New York: Plenum Press.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.Google Scholar
Besharse, J.C. (1982). The daily light-dark cycle and rhythmic metabolism in the photoreceptor and pigment epithelium complex. Progress in Retinal Research 2, 81–118.Google Scholar
Besharse, J.C. & Iuvone, P.M. (1983). Circadian clock in Xenopus eye controlling retinal serotonin N-acetyltransferase. Nature (London) 305, 133–135.Google 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
Burnside, B. & Nagle, B. (1983). Retinomotor movements of photoreceptors and retinal pigment epithelium: Mechanisms and regulation. Progress in Retinal Research 2, 67–109.Google Scholar
Cahill, G.M. & Besharse, J.C. (1990). Dopaminergic regulation of the circadian clock controlling melatonin synthesis in cultured Xenopus eyecups. Investigative Ophthalmology and Visual Science 31, 7.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. (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, 1006–1021.Google 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
De Juan, J., Iniguez, C. & Dowling, J.E. (1991). Nematosomes in external horizontal cells of white perch (Roccus americana) retina: Changes during dark and light adaptation. Brain Research 546, 176–180.Google Scholar
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.Google Scholar
Douglas, R.H. & Wagner, H.-J. (1982). Endogenous patterns of photomechanical movements in teleosts and their relation to activity rhythms. Ceil and Tissue Research 266, 133–144.Google Scholar
Douglas, R.H. & Wagner, H.-J. (1983). Endogenous control of spinule formation in horizontal cells of the teleost retina. Cell and Tissue Research 229, 443–449.Google Scholar
Douglas, R.H., Wagner, H.-J., Zaunreiter, M., Behrens, U.D. & Djamgoz, M.B.A. (1992). The effect of dopamine depletion on lightevoked and circadian retinomotor movements in the teleost retina. Visual Neuroscience 9, 335–343.Google Scholar
Dubocovich, M.L., Lucas, R.C. & Takahashi, J.S. (1985). Light-dependent regulation of dopamine receptors in mammalian retinae. Brain Research 335, 321–325.Google Scholar
Ebbesson, S.O.E. & Meyer, D.L. (1981). Efferents to the retina have multiple sources in teleost fish. Science (New York) 214, 924–928.Google Scholar
Kirsch, M., Djamgoz, M.B.A. & Wagner, H.-J. (1990). Correlation of spinule dynamics and plasticity of the horizontal cell spectral response in cyprinid fish retina: Quantitative analysis. Cell and Tissue Research 260, 123–130.CrossRefGoogle Scholar
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.Google Scholar
Kohler, K. & Weiler, R. (1990a). 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.Google Scholar
Kohler, K. & Weiler, R. (1990b). Influence of cAMP and PKC on spinule formation in the fish retina. Investigative Ophthalmology and Visual Science 31, 333.Google 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.Google Scholar
Kolbinger, W., Kohler, K., Oetting, H. & Weiler, 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
Korenbrot, J.I. & Fernald, R.D. (1989). Circadian rhythm and light regulate opsin mRNA in rod photoreceptors. Nature (London) 337, 454–457.Google Scholar
Kunz, Y.W. (1989). Ontogeny of retinal pigment epithelium-photoreceptor complex and development of rhythmic metabolism under ambient light conditions. Progress in Retinal Research 8Google Scholar
Kunz, Y.W. & Ennis, S. (1983). Ultrastructural diurnal changes of the retinal photoreceptors in the embryo of the viviparous teleost (Poecilia reticulata P.). Cell Differentiation 13, 115–123.Google Scholar
Kunz, Y.W., McCormack, C. & Hayden, T. (1986). Diurnal rhythm of c-AMP in the eye of the trout, Salmo trutta. Cell Biology International Reports 10, 763.Google Scholar
Levinson, G. & Burnside, B. (1981). Circadian 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
McMahon, D.G., Knapp, A. & Dowling, J.E. (1989). Horizontal cell gap junctions: Single channel conductance and modulation by dopamine. Proceedings of the National Academy of Sciences of the U.S.A. 86, 7639–7643.Google Scholar
Negishi, K., Teranishi, T. & Kato, S. (1982). Neurotoxic destruction of dopaminergic cells in the carp retina revealed by a histofluorescence study. Acta Histochemica and Cytochemica 15, 768–778.Google Scholar
Nowak, S.Z. & Zurawska, E. (1989). Dopamine in the rabbit retina and striatum: Diurnal rhythm and effect of light stimulation. Journal of Neural Transmission 75, 201–212.CrossRefGoogle ScholarPubMed
O'Connor, P.M., Kropf, R.B. & Dowling, J.E. (1989). Catechol-amine-sensitive adenylate cyclase in the white perch (Roccus americanus) retina: Evidence for β-adrenergic and dopamine receptors to adenylate cyclase. Journal of Neurochemistry 53, 969–975.Google Scholar
Porceddu, M., DeMontis, G., Mele, S., Ongini, E. & Biggio, G. (1987). D1 dopamine receptors in the rat retina: Effect of dark adaptation and chronic blockade by SCH 23390. Brain Research 424, 264–271.Google Scholar
Schulz, K., Kohler, K. & Weher, R. (1991). Glutamate receptor subtypes and synaptic plasticity in carp horizontal cells. Investigative Ophthalmology and Visual Science 32, 1263.Google Scholar
Stell, W.K., Walker, S.E., Chohan, K.S. & Ball, A.K. (1984). The goldfish nervus terminalis: A luteinizing hormone-releasing hormone and molluscan cardioexcitatory peptide immunoreactive olfactoretinal pathway. Proceedings of the National Academy of Sciences of the U.S.A. 81, 940–944.Google Scholar
Stell, W.K., Walker, S.E. & Ball, A.K. (1987). Functional-anatomical studies on the terminal nerve projection to the retina of bony fishes. Annals of the New York Academy of Sciences 519, 80–96.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.Google Scholar
Tornquist, 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
Uchiyama, H. (1989). Centrifugal pathways to the retina: Influence of the optic tectum. Visual Neuroscience 3, 183–206.CrossRefGoogle Scholar
Wagner, H.-J. (1973). Darkness-induced reduction of the number of synaptic ribbons in fish retina. Nature New Biology 246, 53–55.Google Scholar
Wagner, H.-J. (1975). Quantitative changes of synaptic ribbons in the cone pedicles of Nannacara: Light-dependent or governed by a circadian rhythm? In Vision in Fishes: New Approaches in Research, ed Ali, M.A., pp. 679–686. New York: Plenum Press.Google Scholar
Wagner, H.-J. (1980). Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas. Journal of Neurocytology 9, 575–590.Google Scholar
Wagner, H.-J. & Ali, M.A. (1977). Cone synaptic ribbons and retinomotor changes in the brook trout, Salvelinus fontinalis (Salmonidae, Teleostei), under various experimental conditions. Canadian Review of Zoology 55, 1684–1691.Google Scholar
Weiler, R. & Wagner, H.-J. (1984). Light-dependent change of cone-horizontal cell interactions in carp retina. Brain Research 298, 1–9.Google Scholar
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., Kolbinger, W., Wolburg, H., Kurz-Isler, G. & Wagner, H.-J. (1988b). Dopaminergic neuromodulation in the retinas of lower vertebrates. Neuroscience Research (Suppl.) 8, S183–S196.Google Scholar
Welsh, J.H. & Osborn, C.M. (1937). Diurnal changes in the retina of the catfish, Ameiurus nebulosus. Journal of Comparative Neurology 66, 349–366.Google Scholar
Winfree, A.T. (1987). The Timing of Biological Clocks. New York: Scientific American Library, Freeman.Google Scholar
Wirz-Justice, A., da Prada, M. & Reme, C. (1984). Circadian rhythm in rat retinal dopamine. Neuroscience Letters 45, 21–25.Google Scholar
Wolburg, H. & Kurz-Isler, G. (1988). The light sensitivity of gap-junction structure in retinal horizontal cells is dependent on the intact optic nerve. European Journal of Neuroscience (Suppl.) 1, 152.Google Scholar
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
Zucker, C.L. & Dowling, J.E. (1987). Centrifugal fibres synapse on dopaminergic interplexiform cells in the teleost retina. Nature (London) 330, 166–168.Google Scholar