Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T12:37:43.230Z Has data issue: false hasContentIssue false
  • English
  • Français

Actions of GABAergic ligands on brisk ganglion cells in the cat retina

Published online by Cambridge University Press:  02 June 2009

Frank Müller ,
Reimund Boos  and
Heinz Wässle
Frank Müller
Affiliation:
Max-Planck Institut für Hirnforschung, Frankfurt, Germany
Reimund Boos
Affiliation:
Max-Planck Institut für Hirnforschung, Frankfurt, Germany
Heinz Wässle
Affiliation:
Max-Planck Institut für Hirnforschung, Frankfurt, Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

Gamma-aminobutyric acid (GABA) is the major inhibitory neurotransmitter in the mammalian retina. We tested the actions of iontophoretically applied GABAergic ligands on the spontaneous and stimulus-evoked activity of retinal ganglion cells recorded extracellularly in the in vivo cat eye.

GABA as well as GABAA receptor agonists inhibited all brisk ganglion cell types. This action was antagonized by bicuculline. Bicuculline on its own increased the activity of ON-ganglion cells but suppressed OFF-ganglion cells. This suppression effect was abolished during the blockade of glycinergic transmission by strychnine.

The GABAB receptor agonist baclofen inhibited OFF-ganglion cells whereas the activity of ON-ganglion cells was either increased or decreased depending on the stimulus contrast. The antagonists, phaclofen and 2-hydroxy saclofen, produced opposite effects to baclofen and antagonized its action.

The present study demonstrates that both GABAA and GABAB receptors modulate the activity of ON- and OFF-ganglion cells in the cat retina.

Keywords

RetinaIontophoresisGABAA-receptorsGABAB-receptorsGanglion cells
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 3-4 , October 1992 , pp. 415 - 425
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

Bai, S.H. & Slaughter, M.M. (1989). Effects of baclofen on transient neurons in the mudpuppy retina: Electrogenic and network actions. Journal of Neurophysiology 61, 382–389.Google Scholar
Baumfalk, U. & Albus, K. (1988). Phaclofen antagonizes baclofen induced suppression of visually evoked responses in the cat's striate cortex. Brain Research 463, 398–492.CrossRefGoogle ScholarPubMed
Bolz, J., Frumkes, T., Voigt, T. & Wässle, H. (1985). Action and localization of γ-aminobutyric acid in the cat retina. Journal of Physiology 362, 369–393.CrossRefGoogle ScholarPubMed
Bonanno, G., Pellegrine, G., Asaro, D., Fontana, G. & Raiteri, M. (1989). GABAB autoreceptors in rat cortex synaptosomes: Response under different depolarizing and ionic conditions. European Journal of Pharmacology 172, 41–49.CrossRefGoogle ScholarPubMed
Boos, R., Müller, F. & Wässle, H. (1990). Actions of excitatory amino acids on brisk ganglion cells in the cat retina. Journal of Neurophysiology 64, 1368–1379.Google Scholar
Bormann, J. (1988). Electrophysiology of GABAA and GABAB receptor subtypes. Trends in Neurosciences 11, 112–116.CrossRefGoogle ScholarPubMed
Bowery, N. (1989). GABAB receptors and their significance in mammalian pharmacology. Trends in Pharmacology 10, 401–407.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology 240, 397–419.Google Scholar
Brecha, N. (1983). Retinal neurotransmitters: Histochemical and biochemical studies. In Chemical Neuroanatomy, ed. Emson, P.C., pp. 85–129. New York: Raven Press.Google Scholar
Brecha, N., Lai, M. & Sternini, C. (1990). Differential expression of GABAA α1 and α2 receptor mRNAs in the rat retina. Investigative Ophthalmology and Visual Science (Suppl.) 31, 330.Google Scholar
Brecha, N. & Weigmann, C. (1990). GABAA α and β subunit immunoreactivities in the rabbit retina. Society of Neuroscience Abstracts 16, 1075.Google Scholar
Chun, M.H. & Wässle, H. (1989). GABA-like immunoreactivity in the cat retina. Electron microscopy. Journal of Comparative Neurology 279, 55–67.Google Scholar
Cleland, B.G. & Levick, W.R. (1974). Brisk and sluggish concentrically organized ganglion cells in the cat's retina. Journal of Physiology 240, 421–456.Google Scholar
Dutar, P. & Nicoll, R.A. (1988a). A physiological role for GABAB receptors in the central nervous system. Nature 332, 156–158.CrossRefGoogle ScholarPubMed
Dutar, P. & Nicoll, R.A. (1988b). Pre- and postsynaptic GABAB receptors in the hippocampus have different pharmacological properties. Neuron 1, 585–591.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.Google Scholar
Friedman, D.L. & Redburn, D.A. (1990). Evidence for functionally distinct subclasses of γ-aminobutyric acid receptors in rabbit retina. Journal of Neurochemistry 55, 1189–1199.CrossRefGoogle ScholarPubMed
Frumkes, T.E., Voigt, T. & Wässle, H. (1984). Functional organization of GABA and glycine input to cat retinal ganglion cells. Society for Neuroscience Abstracts 10, 20.Google Scholar
Grünert, U. & Wässle, H. (1990). GABA-like immunoreactivity in the macaque monkey retina: A light and electron microscopic study. Journal of Comparative Neurology 297, 509–524.Google Scholar
Huba, R. & Hofmann, H.D. (1991). Transmitter-gated currents of GABAergic amacrine-like cells in chick retinal cultures. Visual Neuroscience 6, 303–314.Google Scholar
Hughes, T.E., Grünert, U. & Karten, H.J. (1991). GABAA receptors in the retina of the cat: An immunohistochemical study of wholemounts, sections, and dissociated cells. Visual Neuroscience 6, 229–238.CrossRefGoogle Scholar
Hughes, T.E., Russel, G.C., Vitorica, I., DeBlas, A. & Karten, H.J. (1989). Immunohistochemical localization of GABAA receptors in the retina of the New World primate Saimiri Sciureus. Visual Neuroscience 2, 565–581.Google Scholar
Ikeda, H., Hankins, M.W. & Kay, C.D. (1990). Actions of baclofen and phaclofen upon ON- and OFF-ganglion cells in the cat retina. European Journal of Pharmacology 190, 1–9.Google Scholar
Ikeda, H. & Sheardown, M.J. (1983). Transmitters mediating inhibitions of ganglion cells in the cat retina. Iontophoretic studies in vivo. Neuroscience 8, 837–853.CrossRefGoogle ScholarPubMed
Ishida, A. (1989). GABA-activated currents in ganglion cells isolated from goldfish retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 349–361. Berlin, Germany: Springer Verlag.CrossRefGoogle Scholar
Kaneko, A. & Tachibana, M. (1987). GABA mediates the negative feedback from amacrine to bipolar cells. Neuroscience Research (Suppl.) 6, 239–252.Google ScholarPubMed
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860–876.CrossRefGoogle ScholarPubMed
Kerr, D.I.B., Ong, J., Johnston, G.A.R., Abbenante, J. & Prager, R.H. (1988). 2-Hydroxy-Saclofen: An Improved Antagonist At Central And Peripheral GabaB Receptors. Neuroscience Letters 92, 92–96.Google Scholar
Kerr, D.I.B., Ong, J., Prager, R.H., Gynther, B.D. & Curtis, D.R. (1987). Phaclofen: A peripheral and central baclofen antagonist. Brain Research 405, 150–154.CrossRefGoogle ScholarPubMed
Levick, W.R. (1972). Another tungsten microelectrode. Medical and Biological Engineering 10, 510–515.Google Scholar
Lipton, S.A. (1989). GABA-activated single channel currents in out-side-out membrane patches from rat retinal ganglion cells. Visual Neuroscience 3, 275–279.CrossRefGoogle Scholar
Maguire, G., Maple, B., Lukasiewicz, P. & Werblin, F. (1989). γ-Aminobutyrate type B receptor modulation of L-type calcium channel current at bipolar cell terminals in the retina of the tiger salamander. Proceedings of the National Academy of Sciences of the U.S.A. 83, 10144–10147.Google Scholar
Massey, S.C. & Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress in Neurobiology 28, 55–96.Google Scholar
Mosinger, J.L., Yazulla, S. & Studholme, K.M. (1986). GABA-like immunoreactivity in the vertebrate retina: A species comparison. Experimental Eye Research 41, 631–644.Google Scholar
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 1657–1762.CrossRefGoogle ScholarPubMed
Neal, M.J. & Shah, M.A. (1989). Baclofen and phaclofen modulate GABA release from slices of rat cerebral cortex and spinal cord but not from retina. British Journal of Pharmacology 98, 105–112.CrossRefGoogle Scholar
Peichl, L. & Wässle, H. (1979). Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. Journal of Physiology 291, 117–141.Google Scholar
Pittaluga, A., Asaro, D., Pellegrini, G. & Raiteri, M. (1987). Studies on [3H]-GABA and endogenous GABA release in rat cerebral cortex suggest the presence of autoreceptors of the GABAB type. European Journal of Pharmacology 144, 45–52.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1985). A combined Golgi and autoradiographic study of [3H]-glycine-accumulating amacrine cells in the cat retina. Journal of Comparative Neurology 233, 473–480.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1987). Visualization of endogenous glycine in cat retina: An immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 1189–1197.Google Scholar
Pourcho, R.G. & Owczarzak, M.T. (1989). Distribution of GABA immunoreactivity in the cat retina: A light- and electron-microscopic study. Visual Neuroscience 2, 425–435.Google Scholar
Priest, T.D., Robbins, J. & Ikeda, H. (1985). The action of inhibitory neurotransmitters γ-aminobutyric acid and glycine may distinguish between the area centralis and the peripheral retina in cats. Vision Research 26, 1761–1770.Google Scholar
Raiteri, M., Bonanno, G. & Fedele, E. (1989). Release of γ[3H]-aminobutyric acid (GABA) from electrically stimulated rat cortical slices and its modulation by GABAB autoreceptors. Journal of Pharmacology and Experimental Therapeutics 250, 648–652.Google ScholarPubMed
Richards, J.G., Schoch, P., Häring, P., Takacs, B. & Möhler, H. (1987). Resolving GABAA/benzodiazepine receptors: Cellular and subcellular localization in the CNS with monoclonal antibodies. Journal of Neuroscience 7, 1866–1886.CrossRefGoogle ScholarPubMed
Schmidt, M., Humphrey, M.F. & Wässle, H. (1987). Action and localization of acetylcholine in the cat retina. Journal of Neurophysiology 58, 997–1015.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Bai, S.H. (1989). Differential effects of baclofen on sustained and transient cells in the mudpuppy retina. Journal of Neurophysiology 61, 374–381.Google Scholar
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Reviews in Neuroscience 6, 148–185.Google Scholar
Strettoi, E., Dacheux, R.F. & Raviola, E. (1990). Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. Journal of Comparative Neurology 295, 449–466.Google Scholar
Suzuki, S., Tachibana, M. & Kaneko, A. (1990). Effects of glycine and GABA on isolated bipolar cells of the mouse retina. Journal of Physiology 412, 645–662.Google Scholar
Tachibana, M. & Kaneko, A. (1988). Retinal bipolar cells receive negative feedback input from GABAergic amacrine cells. Visual Neuroscience 1, 297–395.CrossRefGoogle ScholarPubMed
Tauck, D.L., Frosch, M.P. & Lipton, S.A. (1988). Characterization of GABA- and glycine-induced currents of solitary rodent retinal ganglion cells in culture. Neuroscience 27, 193–203.Google Scholar
Wässle, H. & Boos, R. (1992). Voltage- and transmitter-gated currents of All-amacrine cells in a slice preparation of the rat retina. Investigative Ophthalmology and Visual Science (ARVO Abstract) 33, 2405.Google Scholar
Wässle, H. & Chun, M.H. (1989). GABA-like immunoreactivity in the cat retina: Light microscopy. Journal of Comparative Neurology 279, 43–54.Google Scholar
Wässle, H., Chun, M.H. & Müller, F. (1987). Amacrine cells in the ganglion cell layer of the cat retina. Journal of Comparative Neurology 265, 391–408.CrossRefGoogle ScholarPubMed
Yeh, H.H., Lee, M.B. & Cheun, J.E. (1990). Properties of GABA-activated whole-cell currents in bipolar cells of the rat retina. Visual Neuroscience 4, 349–357.Google Scholar