Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-22T21:21:09.777Z Has data issue: false hasContentIssue false
  • English
  • Français

Short-term effects of dopamine on photoreceptors, luminosity- and chromaticity-horizontal cells in the turtle retina

Published online by Cambridge University Press:  02 June 2009

Josef Ammermüller ,
Reto Weiler  and
Ido Perlman
Josef Ammermüller
Affiliation:
Department of Neurobiology, University of Oldenburg, Oldenburg, Germany
Reto Weiler
Affiliation:
Department of Neurobiology, University of Oldenburg, Oldenburg, Germany
Ido Perlman
Affiliation:
The Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology and The Rappaport Institute, Haifa, Israel
Get access Rights & Permissions [Opens in a new window]

Abstract

The effects of dopamine on luminosity-type horizontal cells have been documented in different vertebrate retinas, both in vivo and in vitro. Some of these effects may reflect direct action of dopamine onto these cells, but indirect effects mediated by presynaptic neurons cannot be ruled out. Furthermore, direct effects of dopamine on horizontal cells may affect other, postsynaptic neurons in the outer plexiform layer. To test these possibilities, we studied the effects of dopamine on photoreceptors and all types of horizontal cells in the turtle (Pseudemys scripta elegans) retina. Receptive-field properties, responsiveness to light, and time course of light responses were monitored with intracellular recordings. Dopamine at a concentration of 40 μM exerted effects with two different time courses. “Short-term” effects were fully developed after 3 min of dopamine application and reversed within 30 min of washout of the drug. “Long-term” effects were fully developed after about 7–10 min and could not be washed out during the course of our experiments. Only the “short-term” effects were studied in detail in this paper. These were expressed in a reduction of the receptive-field size of all types of horizontal cells studied; L1 and L2 luminosity types as well as Red/Green and Yellow/Blue chromaticity types. The L1 horizontal cells did not exhibit signs of reduced responsiveness to light under dopamine, while in the L2 cells and the two types of chromaticity cells responsiveness decreased. None of the rods, long-wavelength-sensitive, or medium-wavelength-sensitive cones exhibited any apparent reduction in their receptive-field sizes or responsiveness to light. The present results suggest that the “short-term” effects of dopamine are not mediated by photoreceptors and are probably due to direct action of dopamine on horizontal cells.

Keywords

Outer plexiform layerReceptive fieldLight adaptationGap junctionsNetworks
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 3 , May 1995 , pp. 403 - 412
Copyright
Copyright © Cambridge University Press 1995

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

Ammermüller, J., Möckel, W. & Rujan, P. (1993). Geometrical characterization of horizontal cell networks in the turtle retina. Brain Research 616, 351–356.CrossRefGoogle Scholar
Ammermüller, J., Muller, J. & Kolb, H. (1995). The organization of the turtle retina. II. Analysis of colour coded and directional selective cells. Journal of Comparative Neurology (accepted).Google ScholarPubMed
Burkhardt, D.A. (1993). Synaptic feedback, depolarization, and color opponency in cone photoreceptors. Visual Neuroscience 10, 981–989.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 (London) 414, 351–375.CrossRefGoogle ScholarPubMed
Djamgoz, M.B.A. & Wagner, H.-J. (1992). Localization and function of dopamine in the adult vertebrate retina. Neurochemistry International 20, 139–191.Google Scholar
Dong, C.J. & McReynolds, J.C. (1991). The relationship between light, dopamine release and horizontal cell coupling in the mudpuppy retina. Journal of Physiology (London) 440, 291–309.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Belknap Press of Harvard University Press.Google Scholar
Dowling, J.E. (1991). Retinal neuromodulation: The role of dopamine. Visual Neuroscience 7, 87–97.Google Scholar
Fuortes, M.G.F. & Simon, E.J. (1974). Interactions leading to horizontal cell responses in the turtle retina. Journal of Physiology (London) 240, 177–198.CrossRefGoogle ScholarPubMed
Gerschenfeld, H.M., Neyton, J., Piccolino, M. & Witkovsky, P. (1982). L-horizontal cells of the turtle: network organization and coupling modulation. Biomedical Research 3, 21–32.Google Scholar
Golard, A., Witkovsky, P. & Tranchina, D. (1992). Membrane currents of horizontal cells isolated from turtle retina. Journal of Neurophysiology 68, 351–361.CrossRefGoogle ScholarPubMed
Hampson, E.C.G.M., Weiler, R. & Vaney, D. (1994). PH-gated dopaminergic modulation at horizontal cell gap junctions in mammalian retina. Proceedings of the Royal Society B (London) 255, 62–67.Google Scholar
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, 27–55.Google ScholarPubMed
Knapp, A.G. & Dowling, J.E. (1987). Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 325, 437–439.Google Scholar
Knapp, A.G., Schmidt, K.F. & Dowling, J.E. (1990). Dopamine modulates the kinetics of ion channels gated by excitatory amino acids in retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 87, 767–771.Google Scholar
Kolb, H. (1982). The morphology of the bipolar cells, amacrine cells, and ganglion cells in the retina of the turtle Pseudemys scripta elegans. Philosophical Transactions of the Royal Society B (London) 298, 355–393.Google ScholarPubMed
Kolb, H., Cline, C., Wang, H.H. & Brecha, N. (1987). Distribution and morphology of dopaminergic amacrine cells in the retina of the turtle (Pseudemys scripta elegans). Journal of Neurocytology 16, 577–588.Google Scholar
Kolb, H., Perlman, I. & Normann, R.A. (1988). Neural organization of the retina of the turtle Mauremys caspica: A light-microscope and Golgi study. Visual Neuroscience 1, 47–72.Google Scholar
Krizaj, D. & Witkovsky, P. (1993). Effects of submicromolar concentrations of dopamine on photoreceptor to horizontal cell communication. Brain Research 627, 122–128.CrossRefGoogle ScholarPubMed
Kruse, M. & Schmidt, K.F. (1993). Studies on the dopamine-dependent modulation of amino acid-gated currents in cone horizontal cells of the perch (Perca fluviatilis). Vision Research 33, 2031–2042.CrossRefGoogle ScholarPubMed
Lamb, T.D. (1976). Spatial properties of horizontal cell responses in the turtle retina. Journal of Physiology (London) 263, 239–255.CrossRefGoogle ScholarPubMed
Lamb, T.D. & Simon, E.J. (1976). The relation between intercellular coupling and electrical noise in turtle photoreceptors. Journal of Physiology (London) 263, 257–286.CrossRefGoogle ScholarPubMed
Lankheet, M.J.M., Frens, M.A. & van de Grind, W.A. (1990). Spatial properties of horizontal cell responses in the cat retina. Vision Research 30, 1257–1275.Google Scholar
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
Laufer, M. (1982). Electrophysiological studies of drug actions on horizontal cells. In The S-Potential, ed. Drujan, E.D. & Laufer, M., pp. 257–279. New York: Alan R. Liss, Inc.Google Scholar
Leeper, H.F. (1978 a). Horizontal cells of the turtle retina. I. Light microscopy of Golgi preparations. Journal of Comparative Neurology 182, 777–794.Google Scholar
Leeper, H.F. (1978 b). Horizontal cells of the turtle retina. II. Analysis of interconnections between photoreceptor cells and horizontal cells by light microscopy. Journal of Comparative Neurology 182, 795–810.CrossRefGoogle ScholarPubMed
Leeper, H.F. & Copenhagen, D.R. (1979). Mixed rod-cone responses in horizontal cells of snapping turtle retina. Vision Research 19, 407–412.Google Scholar
Leeper, H.F. & Copenhagen, D.R. (1982). Horizontal cells in turtle retina: Structure, synaptic connections and visual processing. In The S-Potential, ed. Drujan, B. & Laufer, M., pp. 77–104. New York: Alan R. Liss, Inc.Google Scholar
Lipetz, L.E. (1985). Some neuronal circuits of the turtle retina. In The Visual System, ed. Fein, A. & Levine, J.S., pp. 107–132. New York: Alan R. Liss, Inc.Google Scholar
Mangel, S.C. & Dowling, J.E. (1985). Responsiveness and receptivefield size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 229, 1107–1109.CrossRefGoogle 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 Scholar
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.CrossRefGoogle ScholarPubMed
Ohtsuka, T. (1983). Axons connecting somata and axon terminals of luminosity-type horizontal cells in the turtle retina: Receptive-field studies and intracellular injections of HRP. Journal of Comparative Neurology 220, 191–198.Google Scholar
Ohtsuka, T. & Kouyama, N. (1986 a). Electron-microscope study of synaptic contacts between photoreceptors and HRP-filled horizontal cells in the turtle retina. Journal of Comparative Neurology 250, 141–156.CrossRefGoogle Scholar
Ohtsuka, T. & Kouyama, N. (1986 a). Physiological and morphological studies of cone-horizontal cell connections in the turtle retina. Neuroscience Research (Suppl.) 4, S69–S84.Google Scholar
Owen, W.G. & Hare, W.A. (1989). Signal transfer from photoreceptors to bipolar cells in the retina of the tiger salamander. Neuroscience Research (Suppl.) 10, S77–S88.Google ScholarPubMed
Perlman, I. & Normann, R.A. (1979). Short-wavelength input to luminosity-type horizontal cells in the turtle retina. Vision Research 19, 903–906.Google Scholar
Perlman, I. & Ammermüller, J. (1994). Lateral spread of visual signals in the L1-horizontal cell syncytium in the turtle retina. Journal of Neurophysiology 72, 2786–2795.Google Scholar
Perlman, I., Normann, R.A., Itzhaki, A. & Daly, S.J. (1985). Chromatic and spatial information processing by red cones and L-type horizontal cells in the turtle retina. Vision Research 25, 543–549.Google Scholar
Perlman, I., Itzhaki, A., Malik, S. & Alpern, M. (1994). The action spectra of cone photoreceptors in the turtle (Mauremys caspica) retina. Visual Neuroscience 11, 243–252.CrossRefGoogle ScholarPubMed
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1981). Centersurround antagonistic organization in small-field luminosity-horizontal cells of turtle retina. Journal of Neurophysiology 45, 363–375.Google Scholar
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1982). Horizontal cells of the turtle retina: A neurotransmitter control of electrical junctions. Journal of Physiology (Paris) 78, 739–742.Google ScholarPubMed
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1984). Decrease of gap junction permeability induced by dopamine and cyclic adenosine 3′:5′-monophosphate in horizontal cells of turtle retina. Journal of Neuroscience 4, 2477–2488.Google Scholar
Piccolino, M., Witkovsky, P. & Trimarchi, C. (1987). Dopaminergic mechanisms underlying the reduction of electrical coupling between horizontal cells of the turtle retina induced by d-amphetamine, bicuculline, and veratridine. Journal of Neuroscience 7, 2273–2284.Google Scholar
Piccolino, M., Demontis, G., Witkovsky, P., Strettoi, E., Cappagli, G.C., Porceddu, M.L., De Montis, M.G., Pepitoni, S., Biggio, G., Meller, E. & Bowmaker, K. (1989). Involvement of D1 and D2 dopamine receptors in the control of horizontal cell electrical coupling in the turtle retina. European Journal of Neuroscience 1, 247–257.CrossRefGoogle ScholarPubMed
Saito, T., Miller, W.H. & Tomita, T. (1974). C-and L-type horizontal cells in the turtle retina. Vision Research 14, 119–123.Google Scholar
Simon, E.J. (1973). Two types of luminosity-horizontal cells in the retina of the turtle. Journal of Physiology (London) 230, 199–211.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Dearry, A. (1992). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 11, 247–292.Google Scholar
Witkovsky, P., Eldred, W. & Karten, H.J. (1984). Catecholamine and indoleamine-containing neurons in the turtle retina. Journal of Comparative Neurology 228, 247–255.Google Scholar
Witkovsky, P., Stone, S. & Besharse, J. (1988). The effects of dopamine and related ligands on photoreceptor to horizontal cell signal transfer in the Xenopus retina. Biomedical Research 9, 93–107.Google Scholar
Witkovsky, P., Nicholson, C., Rice, M.E., Bohmaker, K. & Meller, E. (1993). Extracellular dopamine concentration in the retina of the clawed frog, Xenopus laevis. Proceedings of the National Academy of Sciences of the U.S.A. 90, 5667–5771.CrossRefGoogle ScholarPubMed
Yang, X.-L., Tornquist, K. & Dowling, J.E. (1988). Modulation of cone horizontal cell activity in the teleost fish retina. II. Role of interplexiform cells and dopamine in regulating light responsiveness. Journal of Neuroscience 8, 2269–2278.CrossRefGoogle ScholarPubMed
Yazulla, S. (1976). Cone input to horizontal cells in the turtle retina. Vision Research 16, 727–735.CrossRefGoogle ScholarPubMed