Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-14T11:14:46.414Z Has data issue: false hasContentIssue false
  • English
  • Français

Properties of GABA-activated whole-cell currents in bipolar cells of the rat retina

Published online by Cambridge University Press:  02 June 2009

Hermes H. Yeh ,
Maria B. Lee  and
Jane E. Cheun
Hermes H. Yeh
Affiliation:
Department of Neurobiology and Anatomy, University of Rochester School of Medicine and Dentistry, Rochester, New York
Maria B. Lee
Affiliation:
Department of Neurobiology and Anatomy, University of Rochester School of Medicine and Dentistry, Rochester, New York
Jane E. Cheun
Affiliation:
Department of Neurobiology and Anatomy, University of Rochester School of Medicine and Dentistry, Rochester, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

This paper describes experiments on GABA-activated whole-cell membrane currents in bipolar cells freshly isolated from the adult rat retina. The main goal was to determine whether bipolar cell responses to GABA could be resolved in terms of mediation by the GABAA receptor, the GABAB receptor, or both. Bipolar cells were isolated by gentle enzymatic dissociation and identified by their distinct morphology. GABA agonists and antagonists were applied focally by pressure and the resultant currents were recorded under whole-cell voltage clamp. In all bipolar cells tested, GABA (0.1–100 μM) induced a monophasic response associated with a conductance increase (IGABA). The shift in reversal potential for IGABA as a function of pipet [CI] paralleled that predicted based on the Nernst equation for Cl−. IGABA was mimicked by muscimol (5–20 μM) and antagonized by bicuculline (20–100 μM). Baclofen (0.1–1.0 mM) produced no apparent conductance change. “Hot spots” of sensitivity to GABA which might be associated with regions of synaptic contact were not found; both the soma and processes of all bipolar cells were responsive to focally applied GABA. Furthermore, all bipolar cells tested responded to glycine.

In conclusion, we have established the presence of GABAA receptors on rat retinal bipolar cells. Our data suggest further that these cells lack GABAB receptors. Finally, our observation that bipolar cells in the rat retina are relatively homogeneous in terms of their sensitivity to GABA and glycine lead us to postulate that the functional significance of the presence of receptors and their distribution on a neuron may be dictated more by the topography of the presynaptic inputs than by its inherent chemosensitivity.

Keywords

Rat retinabipolar cellsGABAGlycineGABAA receptor
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 4 , April 1990 , pp. 349 - 357
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

Agardh, E., Bruun, A., Ehinger, B., Ekstrom, P., Van, Veen T. & Wu, J.-Y. (1987). Gamma-aminobutyric acid- and decarboxylaseimmunoreactive neurons in the retina of different vertebrates. Journal of Comparative Neurology 258, 622–630.CrossRefGoogle ScholarPubMed
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 (London) 396, 75–91.CrossRefGoogle ScholarPubMed
Attwell, D., Mobbs, P., Tessier-Lavigne, M. & Wilson, M. (1987). Neurotransmitter-induced currents in retinal bipolar cells of the axolotl (Ambystoma mexicanum). Journal of Physiology 387, 125–161.CrossRefGoogle ScholarPubMed
Bader, C.R., MacLeish, P.R. & Schwartz, E.A. (1978). Response to light of solitary rod photoreceptors isolated from tiger salamander retina. Proceedings of the National Academy of Sciences of the U.S.A. 75, 3507–3511.CrossRefGoogle ScholarPubMed
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, 382–390.CrossRefGoogle ScholarPubMed
Barres, B.A., Silverstein, B.E., Corey, D.P. & Chun, L.L.Y. (1988). Immunological, morphological, and electrophysiological variation among retinal ganglion cells purified by panning. Neuron 1, 791–803.CrossRefGoogle ScholarPubMed
Blaxter, T.J. & Carlen, P.L. (1985). Presynaptic and postsynaptic effects of baclofen in the rat hippocampal slice. Brain Research 341, 195–199.Google Scholar
Bolz, J., Frumkes, T., Voigt, T. & Wassle, H. (1985). Action and localization of gamma-aminobutyric in the cat retina. Journal of Physiology (London) 362, 369–393.Google Scholar
Caruso, D.M., Owczarzak, M.T., Goebel, D.J., Hazlett, J.C. & Pourcho, R.G. (1989). GABA-immunoreactivity in ganglion cells of the rat retina. Brain Research 476, 129–134.CrossRefGoogle ScholarPubMed
Corey, D.P. & Stevens, C.F. (1983). Science and technology of patch-recording electrodes. In Single-Channel Recording, ed. Sakmann, B. & Neher, E. pp. 53–68. New York: Plenum Press.CrossRefGoogle Scholar
Dutar, P. & Nicoll, R.A. (1988). Presynaptic and postsynaptic GABAB receptors in the hippocampus have different pharmacological properties. Neuron 1, 585–591.CrossRefGoogle ScholarPubMed
Grunert, U., Greferath, U. & Wassle, H. (1989). Rod bipolar cells show protein kinase C-like immunoreactivity in the cat and other mammalian retinae. Society for Neuroscience Abstracts 15, 1209.Google 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 Archives 391, 85–100.CrossRefGoogle ScholarPubMed
Huettner, J.E. & Baughman, R.W. (1986). Primary culture of identified neurons from the visual cortex of postnatal rats. Journal of Neuroscience 6, 3044–3060.CrossRefGoogle ScholarPubMed
Hughes, T.E., Carey, R.G., Vitorica, J., De, Blas A.L. & Karten, H.J. (1989). Immunohistochemical localization of GABAA receptors in the retina of the New World primate Saimiri sciureus. Visual Neuroscience 2, 565–581.CrossRefGoogle ScholarPubMed
Huguenard, J.R. & Alger, B.E. (1986). Whole-cell voltage-clamp Study of the fading GABA-activated currents in acutely dissociated hippocampal neurons. Journal of Neurophysiology 56, 1–18.CrossRefGoogle ScholarPubMed
Ishida, A.T. & Cohen, B.N. (1988). GABA-activated whole-cell currents in isolated retinal ganglion cells. Journal of Neurophysiology 60, 381–396.CrossRefGoogle ScholarPubMed
Kaneko, A., Pinto, L.H. & Tachibana, M. (1989). Transient calcium current of retinal bipolar cells of the mouse. Journal of Physiology (London) 410, 613–629.Google Scholar
Kaneko, A. & Tachieana, M. (1987). GABA mediates the negative feedback from amacrine to bipolar cells. Neuroscience Research (Suppl.) 6, S239–S252.Google ScholarPubMed
Karschin, A. & Wassle, H. (1989). Voltage- and transmitter-gated currents in isolated rod bipolar cells of the rat retina. Society for Neuroscience Abstracts 15, 967.Google Scholar
Kondo, H. & Toyoda, J.-I. (1983). GABA and glycine effects on the bipolar cells of the carp retina. Vision Research 23, 1259–1264.CrossRefGoogle ScholarPubMed
Lipton, S.A. & Tauck, D.L. (1987). Voltage-dependent conductances of solitary ganglion cells dissociated from the rat retina. Journal of Physiology (London) 385, 361–391.Google Scholar
Maguire, G., Lukasiewicz, P. & Werblin, F. (1989). Amacrine cell interactions underlying the response to change in the tiger salamander retina. Journal of Neuroscience 9, 726–735.Google Scholar
Marc, R.E. (1985). The role of glycine in retinal circuitry. In Retinal Transmitters and Modulators: Models for the Brain, ed. Morgan, W.W., pp. 119–158. Boca Raton: CRC Press.Google Scholar
Mariani, A.P., Cosenza-Murphy, D. & Barker, J.L. (1987). GABAergic synapses and benzodiazepine receptors are not identically distributed in the primate retinal. Brain Research 415, 152–157.CrossRefGoogle ScholarPubMed
Massey, S.C. & Redburn, D.A. (1987). Transmitter Circuits in the vertebrate retina. Progress in Neurobiology 28, 55–96.Google Scholar
Miller, R.F., Frumkes, T.E., Slaughter, M. & Dacheux, R.F. (1981 a). Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina, I: Receptors, horizontal cells, bipolars, and G-cells. Journal of Neurophysiology 45, 743–763.CrossRefGoogle ScholarPubMed
Miller, R.F., Frumkes, T.E., Slaughter, M. & Dacueux, R.F. (1981 b). Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina, II: Amacrine and ganglion cells. Journal of Neurophysiology 45, 764–782.Google Scholar
Mosinger, J.L., Yazulla, S. & Studholme, K.M. (1986). GABA-like immunoreactivity in the vertebrate retina: a species comparison. Experimental Eye Research 42, 631–644.CrossRefGoogle ScholarPubMed
Nakamura, Y., McGuire, B.A. & Sterling, P. (1980). Interplexiform cell in cat retina: identification by uptake of gamma-[3H]-aminobutyric acid and serial reconstruction. Proceedings of the National Academy of Sciences of the U.S.A. 77, 658–661.CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S. & Teranishi, T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 94, 247–252.CrossRefGoogle ScholarPubMed
Numann, R.E. & Wong, R.K.S. (1984). Voltage-clamp study of GABA response desensitization in single pyramidal cells dissociated from the hippocampus of adult guinea pigs. Neuroscience Letters 47, 289–294.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1983). Neuronal subpopulations in cat retina which accumulate the GABA agonist, [3H]-muscimol: a combined Golgi and autoradiographic study. Journal of Comparative Neurology 219, 25–35.CrossRefGoogle ScholarPubMed
Redburn, D. & Madtes, P. (1986). Postnatal development of [3H]-GABA-accumulating cells in rabbit retina. Journal of Comparative Neurology 243, 41–57.CrossRefGoogle ScholarPubMed
Richards, J.G., Schoch, P., Haring, P., Takacs, B. & Mahler, H. (1987). Resolving GABAA/benzodiazepine receptors: cellular and subcellular localization in the CNS with monoclonal antibodies. Journal of Neuroscience 7, 1866–1886.Google Scholar
Schnitzer, J. & Rusoff, A.C. (1984). Horizontal cells of the mouse retina contain glutamate acid decarboxylase-like immunoreactivity, during early developmental stages. Journal of Neuroscience 4, 2948–2955.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
Tachibana, M. & Kaneko, A. (1986). Properties and function of GABA-induced responses in turtle photoreceptors. Neuroscience Research (Suppl.) 4, S85–S97.Google Scholar
Tessier-Lavigne, M., Attwell, D., Mobbs, P. & Wilson, M. (1988). Membrane currents in retinal bipolar cells of the axolotl. Journal of General Physiology 91, 49–72.Google Scholar
Vaughn, J.E., Famiglietti, E.V., Barber, R.P., Saito, K., Roberts, E. & Ribak, C.E. (1981). GABAergic amacrine cells in rat retina: immunocytochemical identification and synaptic connectivity. Journal of Comparative Neurology 197, 113–127.CrossRefGoogle ScholarPubMed
Wassle, H. & Chun, M.H. (1988). Dopaminergic and indoleamine accumulating amacrine cells express GABA-like immunoreactivity in the cat retina. Journal of Neuroscience 8, 3383–3394.Google Scholar
Wu, J.Y., Brandon, C., Su, Y.T. & Lam, D.M.K. (1981). Immunocytochemical and autoradiographic localization of GABA system in the vertebrate retina. Molecular and Cellular Biochemistry 39, 229–237.CrossRefGoogle ScholarPubMed
Yazulla, S. (1986). GABAergic mechanisms in the retina. In Progress in Retinal Research, Vol. 5, ed. Osborne, N. & Chader, G., pp. 1–52. Oxford: Pergamon.Google Scholar