Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-26T07:21:51.124Z Has data issue: false hasContentIssue false
  • English
  • Français

The effects of GABA and related drugs on horizontal cells in the isolated turtle retina

Published online by Cambridge University Press:  02 June 2009

Ido Perlman  and
Richard A. Normann
Ido Perlman
Affiliation:
The Rappaport Family Institute for Research in the Medical Sciences and Department of Physiology, Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel
Richard A. Normann
Affiliation:
Departments of Bioengineering, Physiology, and Ophthalmology, The University of Utah, Salt Lake City
Get access Rights & Permissions [Opens in a new window]

Abstract

The role of GABA in the outer plexiform layer of the turtle retina has been examined by intracellular recordings from L- and C-type horizontal cells in the isolated retina preparation.

GABA (1–5 mM) slightly depolarized the L-type horizontal cells, reduced the amplitude of their photoresponses, and slowed down the rate of hyperpolarization during the ON component of the photoresponse. These effects could not be replicated by either muscimol or baclofen. When synaptic transmission from the photoreceptors had been blocked by either kynurenic acid or cobalt ions, GABA depolarized L-type horizontal cells and augmented the remaining photoresponses. Neither muscimol nor baclofen exerted any effect on L-type horizontal cells under these conditions. Nipecotic acid, a competitive inhibitor of the GABA-uptake system, induced effects on turtle L-type horizontal cells which were similar to those exerted by GABA. Thus, the complex GABA effect on turtle L-type horizontal cells seems to represent the summation of at least two actions; an indirect one mediated by the red cones via GABAa-type receptors and a direct one which probably reflects the activation of an electrogenic GABA-uptake system.

GABA (1–5 mM) induced a transient depolarization in C-type horizontal cells but eliminated color opponency in only three cells out of seven studied. This observation is inconsistent with the notion that the only neural mechanism responsible for the chromatic properties of C-type horizontal cells in the turtle retina is a GABAergic negative feedback from the L-type horizontal cells onto the green ones.

Keywords

RetinaHorizontal cellsSynapseNegative feedbackGABA
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 5 , November 1990 , pp. 469 - 477
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

Baylor, D.A., Fuortes, M.G.F. & O'Bryan, P.M. (1971) Receptive fields of cones in the retina of the turtle. Journal of Physiology 214, 265–294.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Hodgkin, A.L. (1973) Detection and resolution of visual stimuli by turtle photoreceptors. Journal of Physiology 234, 163–198.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. (1977) Responses and receptive-field organization of cones in perch retina. Journal of Neurophysiology 40, 53–62.Google Scholar
Burkhardt, D.A. & Hassin, G. (1978) Influence of cones upon the chromatic - and luminosity-type horizontal cells in pikeperch retina. Journal of Physiology 281, 125–137.CrossRefGoogle Scholar
Burkhardt, D.A. & Hassin, G., (1983) Quantitative relations between color-opponent responses of horizontal cells and action spectra of cones. Journal of Neurophysiology 49, 961–975.Google Scholar
Cohen, J.L. (1988) The action of γ-aminobutyric acid on the horizontal cells of the skate retina. Brain Research 455, 366–369.Google Scholar
Coleman, P.A., Massey, S.C. & Miller, R.F. (1986) Kynurenic acid distinguishes kainate and quisqualate receptors in the vertebrate retina. Brain Research 381, 172–175.Google Scholar
Djamgoz, M.B.A. & Ruddock, K.H. (1979) Effects of picrotoxin and strychnine on fish retina S-potentials: evidence for inhibitory control of depolarizing responses. Neuroscience Letters 12, 329–334.Google Scholar
Fuortes, M.G.F. & Simon, E.J. (1974) Interactions leading to horizontal cell responses in the turtle retina. Journal of Physiology 240, 177–198.Google Scholar
Gottesman, J. & Burkhardt, D.A. (1987) Response properties of C-type horizontal cells in the retina of the bowfin. Vision Research 27, 179–189.Google Scholar
Hankins, M. W. & Ruddock, K.H. (1984) Electrophysiological effects of GABA on fish retinal horizontal cells are blocked by bicuculline but not by picrotoxin. Neuroscience Letters 44, 1–6.Google Scholar
Johnston, G.A.R., Krogsgaard-Larsen, P., Stephanson, A.L. & Twitchin, B., (1976) Inhibition of the uptake of GABA and related amino acids in rat brain slices by the optical isomers of nipecotic acid. Journal of Neurochemistry 26, 1029–1032.Google Scholar
Kamermans, M. (1989) The functional organization of the horizontal cell layers in carp retina: an electrophysiological and model study. PhD Thesis.Google Scholar
Kaneko, A. & Tachibana, T. (1985) Electrophysiological measurements of the spectral sensitivity of three types of cones in the carp retina. Journal of Physiology (Japan) 35, 355–365.Google ScholarPubMed
Kaneko, A. & Tachibana, M. (1986) Effects of gamma-aminobutyric acid on isolated cone photoreceptors of the turtle retina. Journal of Physiology 373, 444–461.Google Scholar
Kato, S. (1979) C-type horizontal cell responses to annular stimuli. Experimental Eye Research 28, 627–639.CrossRefGoogle ScholarPubMed
Lam, D.M.-K. & Ayoub, G.S. (1983) Biochemical and biophysical studies of isolated horizontal cells from the teleost retina. Vision Research 23, 433–444.Google Scholar
Lam, D.M.-K., Lasater, E.M. & Naka, K.I. (1978) Gamma-aminobutyric acid: a neurotransmitter candidate for cone horizontal cells of the catfish retina. Proceedings of the National Academy of Sciences of the U.S.A. 75, 6310–6313.Google Scholar
Lasater, E.M., Dowling, J. E. & Ripps, H. (1984) Pharmacological properties of isolated horizontal and bipolar cells from the skate retina. Journal of Neuroscience 4, 1966–1975.Google Scholar
Lasater, E.M., Normann, R.A. & Kolb, H. (1989) Signal integration at the pedicle of turtle cone photoreceptors: an anatomical and electrophysiological study. Visual Neuroscience 2, 553–564.CrossRefGoogle ScholarPubMed
Malchow, R.P. & Ripps, H. (1990) GABA-induced currents of skate horizontal cells reflect an electrogenic-uptake mechanism. Investigative Ophthalmology and Visual Science (Suppl.) 31, 178.Google Scholar
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.-K. (1978) GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–246.Google Scholar
Miller, R.F., Frumkes, T.S., Slaughter, M. & Dacheux, R.F. (1981) Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina, I: Receptors, horizontal cells, bipolar cells, and G cells. Journal of Neurophysiology 45, 743–763.Google Scholar
Murakami, M., Shimoda, Y., Nakayani, K., Miyachi, E.-I. & Watanabe, S.-I. (1982 a) GABA-mediated negative feedback from horizontal cells to cones in carp retina. Japanese Journal of Physiology 32, 911–926.Google Scholar
Murakami, M., Shimoda, Y., Nakayani, K., Miyachi, E.-I. & Watanabe, S.-I. (1982 b) GABA-mediated negative feedback and color opponency in carp retina. Japanese Journal of Physiology 32, 927–935.Google Scholar
Negishi, K. & Drujan, B. D. (1979) Effects of some amino acids on horizontal cells in the fish retina. Journal of Neuroscience Research 4, 351–363.Google Scholar
Normann, R.A., Lipetz, L.E. & Muller, J.F. (1988) Does GABAergic feedback mediate the depolarizing photoresponse of “C-type” horizontal cells in the turtle retina? Investigative Ophthalmology and Visual Science (Suppl.) 29, 224.Google Scholar
Normann, R.A. & Perlman, I. (1990) Background and bleaching adaptation in luminosity type horizontal cells in the isolated turtle retina. Journal of Physiology 421, 321–341.Google Scholar
O'Bryan, P.M. (1973) Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina. Journal of Physiology 230, 199–211.Google Scholar
Perlman, I., Normann, R.A., Chandler, J.P. & Liperz, L. (1990) The effects of calcium ions on L-type horizontal cells in the isolated turtle retina. Visual Neuroscience 4, 53–62.Google Scholar
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1980) Synaptic mechanisms involved in responses of chromaticity horizontal cells of turtle retina. Nature 284, 58–60.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., Neyton, J., Witkovsky, P. & Gerschenfeld, H.M. (1982) Gamma-aminobutyric acid antagonists decrease junctional communication between L-type horizontal cells of the retina. Proceedings of the National Academy of Sciences of the U.S.A. 79, 3673–3675.CrossRefGoogle Scholar
Tachibana, M. & Kaneko, A. (1984) Gamma-aminobutyric acid acts at axon terminals of turtle photoreceptors: difference in sensitivity among cell types. Proceedings of the National Academy of Sciences of the U.S.A. 81, 7961–7964.Google Scholar
Witkovsky, P. & Stone, S. (1987) GABA and glycine modify the balance of rod and cone inputs to horizontal cells in Xenopus retina. Experimental Biology 47, 13–22.Google Scholar
Wu, S.M. & Dowling, J.E. (1980) Effects of GABA and glycine on the distal cells of the cyprinid retina. Brain Research 199, 401–414.Google Scholar
Yang, X.-L. & Wu, S.M. (1989) Effects of prolonged light exposure, GABA, and glycine on horizontal cell responses in tiger salamander retina. Journal of Neurophysiology 61, 1025–1035.Google Scholar
Yazulla, S. (1986) GABAergic mechanisms in the retina. Progress in Retinal Research 5, 1–52.Google Scholar