Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-18T23:06:48.808Z Has data issue: false hasContentIssue false
  • English
  • Français

GABA inhibits ACh release from the rabbit retina: A direct effect or feedback to bipolar cells?

Published online by Cambridge University Press:  02 June 2009

David M. Linn  and
Stephen C. Massey
David M. Linn
Affiliation:
Sensory Sciences Center, Graduate School of Biomedical Sciences, University of Texas Health Science Center, Houston
Stephen C. Massey
Affiliation:
Sensory Sciences Center, Graduate School of Biomedical Sciences, University of Texas Health Science Center, Houston
Get access Rights & Permissions [Opens in a new window]

Abstract

The cholinergic amacrine cells of the rabbit retina may be labeled with [3H]-Ch and the activity of the cholinergic population monitored by following the release of [3H]-ACh. We have tested the effect of muscimol, a potent GABAA agonist, on (1) the light-evoked release of ACh, presumably mediated via bipolar cells, which are known to have a direct input to the cholinergic amacrine cells and (2) ACh release produced by exogenous glutamate analogs that probably have a direct effect on cholinergic amacrine cells. Muscimol blocked the light-evoked release of ACh with an IC50 of 1.0 μM. In contrast, ACh release produced by nonsaturating doses of kainate or NMDA was not reduced even by 100 μM muscimol. Thus, we have been unable to demonstrate a direct effect of GABA on the cholinergic amacrine cells.

GABA antagonists, such as picrotoxin, caused a large increase in the base release and potentiated the light-evoked release of ACh. Both these effects were abolished by DNQX, a kainate antagonist that blocks the input to cholinergic amacine cells from bipolar cells. DNQX blocked the effects of picrotoxin even when controls showed that the mechanism of ACh release was still functional. Together, these results imply that the dominant site for the GABA-mediated inhibition of ACh release is on the bipolar cell input to the cholinergic amacrine cells. This is consistent with previous anatomical and physiological evidence that bipolar cells receive negative feedback from GABA amacrine cells.

Keywords

RetinaACh releaseGABACholinergic amacrine cells
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 2 , February 1992 , pp. 97 - 106
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

Agardh, E., Yeh, H.H., Hermann, R. & Puro, D.G. (1985). γ-Aminobutyric acid-mediated inhibition at cholinergic synapses formed by cultured retinal neurons. Brain Research 330, 323–328.Google Scholar
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.Google Scholar
Ames, A. III & Nesbett, F.B. (1981). In vitro retina as an experimental model of the central nervous system. Journal of Neurochemistry 31, 867–877.Google Scholar
Ariel, M. & Daw, N.W. (1982). Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. Journal of Physiology (London) 324, 135–160.Google Scholar
Bloomfield, S. & 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.Google Scholar
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119–130.Google Scholar
Brandon, C., Lam, D.M.-K. & Wu, J.-Y. (1979). The γ-aminobutyric acid system in the rabbit retina: Localization by immunocytochemistry and autoradiography. Proceedings of the National Academy of Sciences of the U.S.A. 76, 3557–3561.Google Scholar
Brecha, N., Johnson, D., Peichl, L. & Wassle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 6187–6191.Google Scholar
Brecha, N. & Weigmann, C. (1990). GABAAα and β subunit immunoreactivities in the rabbit retina. Society for Neuroscience Abstracts 16, 1075.Google Scholar
Chun, M.-H., Wassle, H. & Brecha, N. (1988). Colocalization of [3H]-muscimol and cholineacetyltransferase immunoreactivity in amacrine cells of the cat retina. Neuroscience Letters 94, 259–263.CrossRefGoogle 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
Cunningham, J.R. & Neal, M.J. (1983). Effect of GABA agonists, glycine, taurine and neuropeptides on acetylcholine release from rabbit retina. Journal of Physiology (London) 336, 553–577.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 (London) 366, 47–62.Google Scholar
Ehinger, B. & Falck, B. (1971). Autoradiography of some suspected neurotransmitter substances: GABA, glycine, glutamic acid, histamine, dopamine and L-DOPA. Brain Research 33, 157–172.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.Google Scholar
Famiglietti, E.V. Jr (1983 a). ON and OFF pathways through amacrine cells in mammalian retina: The synaptic connections of ‘star-burst’ amacrine cells. Vision Research 23, 1265–1279.Google Scholar
Famiglietti, E.V. Jr (1983b). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138–144.Google Scholar
Famiglietti, E.V. & Tumosa, N. (1987). Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398–403.Google Scholar
Freed, M.A., Smith, R.G. & Sterling, P. (1987). Rod bipolar array in the cat retina: Pattern of input from rods and GABA-accumulating amacrine cells. Journal of Comparative Neurology 266, 445–455.Google Scholar
Heidelberger, R. & Matthews, G. (1990). Inhibition by GABA of depolarization-induced calcium influx in goldfish retinal bipolar neurons. Society for Neuroscience Abstracts 16, 465.Google Scholar
Honore, T., Davies, S.N., Drejer, J., Fletcher, E.J., Jacobsen, P., Lodge, D. & Nielsen, F.E. (1988). Quinoxalinediones: Potent competitive non-NMDA glutamate receptor antagonists. Science 241, 701–703.Google Scholar
Kaneko, A. & Tachibana, M. (1987). GABA mediates the negative feedback from amacrine to bipolar cells. Neuroscience Research (Suppl.) 6, S239–S252.Google Scholar
Linn, D.M., Blazynski, C., Redburn, D.A. & Massey, S.C. (1991). Acetylcholine release from the rabbit retina mediated by kainate receptors. Journal of Neuroscience 11, 111–122.Google Scholar
Linn, D.M. & Massey, S.C. (1991). Acetylcholine release from the rabbit retina mediated by NMDA receptors. Journal of Neuroscience 11, 123–133.Google Scholar
Lukasiewicz, P.D. & McReynolds, J.S. (1985). Synaptic transmission at the N-methyl-D-aspartate receptors in the proximal retina of the mudpuppy. Journal of Physiology 367, 99–115.Google Scholar
Marc, R.E., Liu, W.-L.S., Kalloniatis, M., Raiguel, S.F. & Van Haesendonck, E. (1990). Patterns of glutamate immunoreactivity in the goldfish retina. Journal of Neuroscience 10, 4006–4034.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, 221–245.Google Scholar
Masland, R.H. & Ames, A.D. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neuro-physiology 39, 1220–1235.Google Scholar
Masland, R.H. & Livingstone, C.J. (1976). Effect of stimulation with light on synthesis and release of acetylcholine by an isolated mammalian retina. Journal of Neurophysiology 39, 1210–1219.Google Scholar
Masland, R.H. & Mills, J.W. (1979). Autoradiographic identification of acetylcholine in the rabbit retina. Journal of Cell Biology 83, 159–178.Google Scholar
Masland, R.H., Mills, J.W. & Cassidy, C. (1984 a). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society B (London) 223, 121–139.Google Scholar
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984 b). Acetylcholine-synthesizing amacrine cells: Identification and selective staining by using radioautography and fluorescent markers. Proceedings of the Royal Society B (London) 223, 79–100.Google Scholar
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399–425.Google Scholar
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.Google Scholar
Massey, S.C. & Miller, R.F. (1990). N-methyl-D-aspartate receptors of ganglion cells in rabbit retina. Journal of Neurophysiology 63, 16–30.Google Scholar
Massey, S.C. & Neal, M.J. (1979). The light-evoked release of acetylcholine from the rabbit retina in vivo and its inhibition by gamma-aminobutyric acid. Journal of Neurochemistry 32, 1327–1329.Google Scholar
Massey, S.C. & Redburn, D.A. (1982). A tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina. Journal of Neuroscience 2, 1633–1643.Google Scholar
Millar, T.J. & Morgan, I.G. (1987). Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells. Neuroscience Letters 74, 281–285.Google Scholar
O'malley, D.M. & Masland, R.H. (1989). Corelease of acetylcholine and gamma-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the U.S.A. 85, 8737–8741.Google Scholar
Slaughter, M.M. & Miller, R.F. (1983). Bipolar cells in the mudpuppy retina use an excitatory amino acid neurotransmitter. Nature 303, 537–538.Google Scholar
Tachibana, M. & Kaneko, A. (1988). Retinal bipolar cells receive negative feedback input from GABAergic amacrine cells. Visual Neuroscience 1, 297–305.Google Scholar
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101–119.Google Scholar
Tauchi, M. & Masland, R.H. (1985). Local order among the dendrites of an amacrine cell population. Journal of Neuroscience 5, 2494–2501.Google Scholar
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society B (London) 220, 501–508.Google ScholarPubMed
Vaney, D.I., Collin, S.P. & Young, H.M. (1989). Dendritic relationships between cholinergic amacrine cells and direction-selective retinal ganglion cells. In Neurobiology of the Inner Retina, NATO ASI Series, Vol. H31, eds. Weiler, R. & Osborne, N.N., pp. 157–168Berlin: Springer-Verlag.Google Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.Google Scholar
Vaughn, J.E., Famiglietti, E.V. Jr, 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.Google Scholar
Wyatt, H.J. & Daw, N.W. (1976). Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. Science 191, 204–205.Google Scholar
Yazulla, S. (1986). GABAergic mechanisms in the retina. Progress in Retinal Research 5, 1–52.Google Scholar
Yazulla, S., Studholme, K.M. & Wu, J.-Y. (1987). GABAergic input to synaptic terminals of mbl bipolar cells in the goldfish retina. Brain Research 411, 400–405.Google Scholar