Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T12:37:29.617Z Has data issue: false hasContentIssue false
  • English
  • Français

Transmitter-gated currents of GABAergic amacrine-like cells in chick retinal cultures

Published online by Cambridge University Press:  02 June 2009

Reiner huba  and
Hans-Dieter Hofmann
Reiner huba
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstrasse 46, W-6000 Frankfurt/M., Germany
Hans-Dieter Hofmann
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstrasse 46, W-6000 Frankfurt/M., Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

A subpopulation of cells developing in dissociated neuronal cultures prepared from 8-day-old embryonic chick retinae can be identified as putative in vitro counterparts of GABAergic amacrine cells by immunocytochemical and autoradiographic markers and by their electrophysiological responses to transmitter agonists. In the present study, transmitter-gated conductances expressed by these neurons were examined using the whole-cell patch-clamp technique. At negative holding potentials, the excitatory amino acid agonists N-methyl-D-aspartate (NMDA), kainate quisqualate, and glutamate induced inward currents with reversal potentials close to 0 mV in most of the cells selected for recording. NMDA-evoked responses were selectively blocked by the noncompetitive inhibitor MK 801 and by Mg2+ (in a voltage-dependent manner) and were potentiated in the presence of submicromolar concentrations of glycine. Glutamate apparently interacted with both NMDA and non-NMDA type receptors. All cells tested responded to the inhibitory transmitters GABA and glycine. Both inhibitory agonists could be shown to activate chloride conductances. Responses to GABA and glycine were specifically inhibited in the presence of bicuculline and strychnine, respectively. Thus, GABAergic neurons in retinal cultures express at least two different excitatory amino acid receptors–NMDA and non-NMDA–and two different inhibitory amino acid receptors–the GABAA and the glycine receptor. The results demonstrate the ability of the cultured neurons to develop an apparently mature phenotype and contribute to the understanding of the functional properties of GABAergic amacrine cells in the vertebrate retina.

Keywords

Chick retinaPatch-clamp recordingExcitatory amino acidsGamma-aminobutyric acidGlycine
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 4 , April 1991 , pp. 303 - 314
Copyright
Copyright © Cambridge University Press 1991

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

Aizenman, E., Frosch, M.P. ' Lipton, S.A. (1988). Responses mediated by excitatory amino-acid receptors in solitary retinal ganglion cells from rat. Journal of Physiology 398, 75–91.CrossRefGoogle Scholar
Ascher, P. ' Nowak, L. (1988). The role of divalent cations in the Nmethyl-D-aspartate responses of mouse central neurons in culture. Journal of Physiology 399, 247–266.CrossRefGoogle Scholar
Ault, B., Evans, R.H., Francis, A.A., Oakes, D.J. ' Watkins, J.C. (1980). Selective depression of excitatory amino-acid-induced depolarizations by magnesium ions in isolated spinal cord preparations. Journal of Physiology 307, 413–428.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. ' Dowling, J.E. (1985). Roles of aspartate and glutamate in synaptic transmission in rabbit retina, II: Inner plexiform layer. Journal of Neurophysiology 53, 714–725.CrossRefGoogle ScholarPubMed
Bormann, J., Hamill, O.P. ' Sakmann, B. (1987). Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurons. Journal of Physiology 385, 243–286.CrossRefGoogle Scholar
Brecha, N.C. (1983). Retinal neurotransmitters: Histochemical and biochemical studies. In Chemical Neuroanatomy, ed. Emson, P.C., pp. 85–129. New York: Raven Press.Google Scholar
Cunningham, J.R. ' Neal, M.J. (1985). Effect of excitatory amino acids and analogues on [3H]-acetylcholine release from amacrine cells of the rabbit retina. Journal of Physiology 366, 47–62.CrossRefGoogle ScholarPubMed
Daw, N.W., Brunken, W.J. ' Parkinson, D. (1989). The function of synaptic transmitters in the retina. Annual Review of Neuroscience 12, 205–241.CrossRefGoogle ScholarPubMed
Ehinger, B. ' Dowling, J.E. (1987). Retinal neurocircuitry and transmission. In Handbook of Chemical Neuroanatomy, Vol. 5, ed. Björklund, A., Hökfelt, T. ' Swanson, L.W., pp. 389–446. Amsterdam, The Netherlands: Elsevier.Google Scholar
Ehinger, B., Ottersen, O.P., Storm-Mathisen, J. ' Dowling, J.E. (1988). Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proceedings of the National Academy of Sciences of the U.S.A. 85, 8321–8325.CrossRefGoogle ScholarPubMed
Fenwick, E.M., Marty, A. ' Neher, E. (1982). A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. Journal of Physiology 331, 577–597.Google Scholar
Foster, A.C. ' Fagg, G.E. (1984). Acidic amino-acid binding sites in mammalian neuronal membranes: their characteristics and relationship to synaptic receptors. Brain Research Reviews 7, 103–164.CrossRefGoogle Scholar
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. ' Sigworth, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Achives 395, 85–100.CrossRefGoogle Scholar
Hofmann, H.-D. (1988). Development of cholinergic retinal neurons from embryonic chicken in monolayer cultures: stimulation by glial cell-derived factors. Journal of Neuroscience 8, 1361–1369.CrossRefGoogle ScholarPubMed
Hofmann, H.-D. ' Möckel, V. (1991). Release of γ-aminobutyric acid from cultured amacrine-like neurons mediated by different excitatory amino-acid receptors. Journal of Neurochemistry (in press).CrossRefGoogle Scholar
Honey, C.R., Miljkovic, Z. ' MacDonald, J.F. (1985). Ketamine and phencyclidine cause a voltage-dependent block of responses to L-aspartic acid. Neuroscience Letters 61, 135–139.CrossRefGoogle Scholar
Huba, R. ' Hofmann, H.-D. (1990). Identification of GABAergic amacrine cell-like neurons developing in chick retinal monolayer cultures. Neuroscience Letters 117, 37–42.CrossRefGoogle ScholarPubMed
Ishida, A.T. ' Neyton, J. (1985). Quisqualate and L-glutamate inhibit retinal horizontal cells responses to kainate. Proceedings of the NationalAcademy of Sciences of the U.S.A. 82, 1837–1841.Google Scholar
Johnson, J.W. ' Ascher, P. (1987). Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529–531.CrossRefGoogle ScholarPubMed
Kaneko, A. ' Tachibana, M. (1985). A voltage-clamp analysis of membrane currents on solitary bipolar cells dissociated from Carassius auratus. Journal of Physiology 358, 139–152.Google Scholar
Karschin, A., Aizenman, E. ' Lipton, S.A. (1988). The interaction of agonists and noncompetitive antagonists at the excitatory amino-acid receptors in rat retinal ganglion cells in vitro. Journal of Neuroscience 8, 2895–2906.CrossRefGoogle 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
Köhr, G. ' Heinemann, U. (1988). Differences in magnesium and calcium effects on N-methyl-D-aspartate- and quisqualate-induced decreases in extracellular sodium concentration in rat hippocampal slices. Experimental Brain Research 71, 425–430.Google Scholar
Lasater, E.M. ' Dowling, J.E. (1982). Carp horizontal cells in culture respond selectively to L-glutamate and its agonists. Proceedings of the National Academy of Sciences of the U.S.A. 79, 936–940.CrossRefGoogle ScholarPubMed
Lipton, S.A. ' Tauck, D.L. (1987). Voltage-dependent conductances of solitary ganglion cells dissociated from rat retina. Journal of Physiology 385, 361–391.Google Scholar
MacDermott, A.B., Mayer, M.L., Westbrook, G.L., Smith, S.J. ' Barker, J.L. (1986). NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurons. Nature 321, 519–522.CrossRefGoogle Scholar
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399–425.CrossRefGoogle Scholar
Massey, S.C. ' Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress in Neurobiology 28, 55–96.CrossRefGoogle ScholarPubMed
Massey, S.C. ' Miller, R.F. (1988). Glutamate receptors of ganglion cells in the rabbit retina: evidence for glutamate as a bipolar cell transmitter. Journal of Physiology 405, 635–655.CrossRefGoogle ScholarPubMed
Mayer, M.L., Westbrook, G.L. ' Guthrie, P.B. (1984). Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurons. Nature 309, 261–263.Google Scholar
Mayer, M.L. ' Westbrook, G.L. (1987 a). The physiology of excitatory amino acids in the vertebrate central nervous system. Progress in Neurobiology 28, 197–276.Google Scholar
Mayer, M.L. ' Westbrook, G.L. (1987 b). Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurons. Journal of Physiology 394, 501–527.CrossRefGoogle Scholar
Miller, R.F. ' Slaughter, M.M. (1985). Excitatory amino-acid receptors in the vertebrate retina. In Retinal Neurotransmitters and Modulators: Models for the Brain, Vol. II, ed. Morgan, W.W., pp. 123–160. Boca Raton, Florida: CRC Press.Google Scholar
Monaghan, D.T., Bridges, R.J. ' Cotman, C.W. (1989). The excitatory amino-acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annual Review of Pharmacology and Toxicology 29, 365–402.CrossRefGoogle ScholarPubMed
Nicoletti, F., Wroblewski, J.T., Novelli, A., Guidotti, A. ' Costa, E. (1986). The activation of inositol phospolipid metabolism as a signal-transducing system for excitatory amino acids in primary cultures of cerebellar granule cells. Journal of Neuroscience 6, 1905–1911.Google Scholar
Nowak, L., Bregestovski, P., Ascher, P., Herbert, A. ' Prochiantz, A. (1984). Magnesium gates glutamate-activated channels in mouse central neurons. Nature 307, 462–465.Google Scholar
O'Brien, R.J. ' Fischbach, G.D. (1986). Characterization of excitatory amino-acid receptors expressed by embryonic chick motoneurons in vitro. Journal of Neuroscience 6, 3275–3283.CrossRefGoogle ScholarPubMed
O'Dell, T.J. ' Christensen, B.N. (1989). Horizontal cells isolated from catfish retina contain two types of excitatory amino-acid receptors. Journal of Neurophysiology 61, 1097–1109.CrossRefGoogle ScholarPubMed
Perouansky, M. ' Grantyn, R. (1989). Separation of quisqualateand kainate-selective glutamate receptors in cultured neurons from the rat superior colliculus. Journal of Neuroscience 9, 70–80.CrossRefGoogle Scholar
Pin, J.P., van Vliet, B.J. ' Bockaert, J. (1988). NMDA- and kainateevoked GABA release from striatal neurons differentiated in primary culture: differential blocking by phencyclidine. Neuroscience Letters 87, 87–92.CrossRefGoogle ScholarPubMed
Pin, J.P., Van Vliet, B.J. ' Bockaert, J. (1989). Complex interactions between quisqualate and kainate receptors as revealed by measurements of GABA release from striatal neurons in primary culture. European Journal of Pharmacology 172, 81–91.CrossRefGoogle ScholarPubMed
Rodriguez-Tébar, A., Jeffrey, P.L., Thoenen, H. ' Barde, Y.-A. (1989). The survival of chick retinal ganglion cells in response to brain-derived neurotrophic factor depends on their embryonic age. Developmental Biology 136, 296–303.Google Scholar
Slaughter, M.M. ' Miller, R.F. (1981). 2-amino-4-phosphonobutyric acid, a new pharmacological tool for retina research. Nature 211, 182–185.Google Scholar
Slaughter, M.M. ' Miller, R.F. (1983). The role of excitatory amino- acid transmitters in the mudpuppy retina: an analysis of kainic acid and N-methyl-aspartate. Journal of Neuroscience 3, 1701–1711.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
Vaney, D.I. (1986). Parallel and serial pathways in the inner plexiform layer of the mammalian retina. In Visual Neuroscience, ed. Pettigrew, J.D., Sanderson, K.J., Levick, W.R., pp. 44–59. Cambridge, England: Cambridge University Press.Google Scholar
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 1–46.CrossRefGoogle Scholar
Watkins, J.C. ' Evans, R.H. (1981). Excitatory amino-acid transmission. Annual Review of Pharmacology and Toxicology 21, 165–204.CrossRefGoogle Scholar
Westbrook, G.L. ' Mayer, M.L. (1984). Glutamate currents in mammalian spinal cord neurons. Resolution of a paradox. Brain Research 301, 375–379.CrossRefGoogle Scholar
Wong, E.H.F., Kemp, J.A., Priestley, T., Knight, A.R., Woodruff, G.N. ' Iversen, L.L. (1986). The anticonvulsant Mk 801 is a potent N-methyl-D-aspartate antagonist. Proceedings of the National Academy of Sciences of the U.S.A. 83, 7104–7108.CrossRefGoogle ScholarPubMed
Yazulla, S. (1986). GABAergic mechanisms in the retina. Progress in Retinal Research 5, 1–52.CrossRefGoogle Scholar
Zorumski, C.F. ' Yang, J. (1988). AMPA, kainate, and quisqualate activate a common receptor-channel complex on embryonic chick motoneurons. Journal of Neuroscience 8, 4277–4286.CrossRefGoogle ScholarPubMed