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Whole-cell currents activated at nicotinic acetylcholine receptors on ganglion cells isolated from goldfish retina

Published online by Cambridge University Press:  02 June 2009

Bruce Yazejian
Affiliation:
Department of Ophthalmology, Jules Stein Eye Institute, UCLA School of Medicine, Los Angeles
Gordon L. Fain
Affiliation:
Department of Physiological Science, Jules Stein Eye Institute, UCLA School of Medicine, Los Angeles

Abstract

We have recorded whole-cell membrane currents in response to exogenously applied acetylcholine (ACh), nicotine, and 1,1 dimethyl-4-phenyl piperazinium iodide on retinal ganglion cells enzymatically dissociated from goldfish retina. Agonist applications induced nicotinic-type responses in a majority of cells when cells were isolated under optimal conditions. Currents were reminiscent of nicotinic-type ganglionic responses. Dose-response measurements of ACh-induced currents indicated an EC50 of 52 μM and a Hill coefficient of 0.6. Currents were selective for Na+ over Cl and were highly inwardly rectifying. Responses were blocked reversibly by d-tubocurarine, hexamethonium chloride, and N-methyl-D-glucamine. In 50% of the cases, α-bungarotoxin reversibly blocked the current induced by ACh application. The blocking action of mecamylamine was irreversible and independent of the presence of agonist but was more effective in the presence of ACh. We conclude that functional nicotinic ACh receptors exist on most goldfish retinal ganglion cells.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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References

Adams, D.J., Dwyer, T.M. & Hille, B. (1980). The permeability of endplate channels to monovalent and divalent metal cations. Journal of General Physiology 75, 493510CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982 a). Effect of cholinergic drugs on receptive-field properties of rabbit retinal ganglion cells. Journal of Physiology 324, 135160CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982 b). Pharmacological analysis of direc-tionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161185CrossRefGoogle ScholarPubMed
Ascher, P., Large, W.A. & Rang, H.P. (1979). Studies on the mechanism of action of acetylcholine antagonists on rat parasympathetic ganglion cells. Journal of Physiology 295, 139170CrossRefGoogle ScholarPubMed
Bean, B.P., Williams, C.A. & Ceelen, P.W. (1990). ATP-activated channels in rat and bullfrog sensory neurons: Current-voltage relation and single-channel behavior. Journal of Neuroscience 10, 1119CrossRefGoogle ScholarPubMed
Bertrand, D., Ballivet, M. & Rungger, D. (1990). Activation and blocking of neuronal nicotinic acetylcholine receptor reconstituted in xenopus oocytes. Proceedings of the National Academy of Sciences of the U.S.A. 87, 19931997CrossRefGoogle ScholarPubMed
Bertrand, D., Devillers-Thiéry, A., Revah, F., Galzi, J.-L., Hussy, N., Mulle, C., Bertrand, S., Ballivet, M. & Changeux, J.-P. (1992). Unconventional pharmacology of a neuronal nicotinic receptor mutated in the channel domain. Proceedings of the National Academy of Sciences of the U.S.A. 89, 12611265CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. Journal of Neuroscience 6, 113CrossRefGoogle Scholar
Bray, D. (1970). Surface movements during the growth of single ex-planted neurons. Proceedings of the National Academy of Sciences of the U.S.A. 65, 905910CrossRefGoogle Scholar
Brown, D.A. & Fumagalli, L. (1977). Dissociation of α-bungarotoxin binding and receptor block in the rat superior cervical ganglion. Brain Research 129, 165168CrossRefGoogle Scholar
Chua, M. & Betz, W.J. (1991). Characterization of ion channels on the surface membrane of adult rat skeletal muscle. Biophysical Journal 59, 12511260CrossRefGoogle ScholarPubMed
Cohen, B.N., Fain, G.L. & Fain, M.J. (1989). GABA and glycine channels in isolated ganglion cells from the goldfish retina. Journal of Physiology 417, 5382CrossRefGoogle Scholar
Daw, N.W. (1968). Colour-coded ganglion cells in the goldfish retina: Extension of their receptive fields by means of new stimuli. Journal of Physiology 197, 567592CrossRefGoogle ScholarPubMed
De La Garza, R., McGuire, T.J., Freedman, R. & Hoffer, B.J. (1987). Selective antagonism of nicotine actions in the rat cerebellum with α-bungarotoxin. Neuroscience 23, 887891CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr, (1983). ON and OFF pathways through amacrine cells in mammalian retina: The synaptic connections of "star-burst" amacrine cells. Vision Research 23, 12651279CrossRefGoogle Scholar
Famiglietti, E.V. (1991). Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction. Journal of Comparative Neurology 309, 4070CrossRefGoogle 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, 577597CrossRefGoogle ScholarPubMed
Fieber, L.A. & Adams, D.J. (1991). Acetylcholine-evoked currents in cultured neurones dissociated from rat parasympathetic cardiac ganglia. Journal of Physiology 434, 215237CrossRefGoogle ScholarPubMed
Glickman, R.D. & Adolph, A.R. (1982). Acetylcholine and substance P: Action via direct receptors on carp retinal ganglion cells. Investigative Ophthalmology and Visual Research 22, 804808Google Scholar
Glickman, R.D., Adolph, A.R. & Dowling, J.E. (1982). Inner plexiform circuits in the carp retina: Effects of cholinergic agonists, GABA, and substance P on the ganglion cells. Brain Research 234 8199CrossRefGoogle ScholarPubMed
Ifune, C.K. & Steinbach, J.H. (1990). Rectification of acetylcholine-elicited currents in PC12 pheochromocytoma cells. Proceedings of the National Academy of Sciences of the U.S.A. 87, 47944798CrossRefGoogle ScholarPubMed
Keyser, K.T., Britto, L.R.G., Schoepfer, R., Whiting, P., Cooper, J., Brozozowska-Prechtl, A., Karten, H.J. & Lindstrom, J. (1992). Alpha-bungarotoxin sensitive nicotinic acetylcholine receptors in chick retina: Identification of three subtypes and immunohistochemical localization. Investigative Ophthalmology and Visual Science (ARVO Suppl.) 33, 1721.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, 111122CrossRefGoogle ScholarPubMed
Linn, D.M. & Massey, S.C. (1991). Acetylcholine release from the rabbit retina mediated by NMDA receptors. Journal of Neuroscience 11, 123133CrossRefGoogle ScholarPubMed
Lipton, S.A., Aizenman, E. & Loring, R.H. (1987). Neuronal nicotinic acetylcholine responses in solitary mammalian retinal ganglion cells. Pflügers Archives 410, 3743CrossRefGoogle ScholarPubMed
Loring, R.H., Andrews, D., Lane, W. & Zigmond, R.E. (1986). Amino acid sequence of toxin F, a snake venom that blocks neuronal nicotinic receptors. Brain Research 36, 3037CrossRefGoogle Scholar
Masland, R.H. & Ames, A. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 12201235CrossRefGoogle Scholar
Masland, R.H., Mills, J.W. & Cassidy, C. (1984). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society B (London) 223, 121139Google ScholarPubMed
Massey, S.C. & Redburn, D.A. (1985). Light-evoked release of acetylcholine in response to a single flash: Cholinergic amacrine cells receive ON and OFF input. Brain Research 328, 374377CrossRefGoogle ScholarPubMed
Mathie, A., Colquhoun, D. & Cull-Candy, S.G. (1990). Rectification of currents activated by nicotinic acetylcholine receptors in rat sympathetic ganglion neurones. Journal of Physiology 427, 625655CrossRefGoogle ScholarPubMed
Mitchell, C.K. & Redburn, D.A. (1991). Melatonin inhibits ACh release from rabbit retina. Visual Neuroscience 7, 479486CrossRefGoogle ScholarPubMed
Neely, A. & Lingle, C.J. (1986). Trapping of an open-channel blocker at the frog neuromuscular acetylcholine channel. Biophysical Journal 50, 981986CrossRefGoogle ScholarPubMed
O’Malley, D.M., Sandell, J.H. & Masland, R.H. (1992). Co-release of acetylcholine and GABA by the starburst amacrine cells. Journal of Neuroscience 12, 13941408CrossRefGoogle ScholarPubMed
Sah, D.W.Y., Loring, R.H. & Zigmond, R.E. (1987). Long-term blockade by toxin F of nicotinic synaptic potentials in cultured sympathetic neurons. Neuroscience 20, 867874CrossRefGoogle ScholarPubMed
Schmidt, M., Humphrey, M.F. & Wassle, H. (1987). Action and localization of acetylcholine in the cat retina. Journal of Neurophysiology 58, 9971015CrossRefGoogle ScholarPubMed
Schwartz, M. & Agranoff, B.W. (1981). Outgrowth and maintenance of neurites from cultured goldfish retinal ganglion cells. Brain Research 206, 331343CrossRefGoogle ScholarPubMed
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, 101119Google ScholarPubMed
Tumosa, N., Eckenstein, F. & Stell, W.K. (1984). Immunological localization of putative cholinergic neurons in the goldfish retina. Neuroscience Letters 48, 255259CrossRefGoogle 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, 501508Google ScholarPubMed
Verino, S., Amador, M., Luetje, C.W., Patrick, J. & Dani, J.A. (1992). Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors. Neuron 8, 127134CrossRefGoogle Scholar
Wartzok, D. & Marks, W.B. (1973). Directionally selective visual units recorded in optic tectum of the goldfish. Journal of Neurophysiology 36, 588604CrossRefGoogle ScholarPubMed
Yakel, J.L., Shao, X.M. & Jackson, M.B. (1990). The selectivity of the channel coupled to the 5-HT3 receptor. Brain Research 533, 4652CrossRefGoogle Scholar
Yawo, H. (1989). Rectification of synaptic and acetylcholine currents in submandibular ganglion cells. Journal of Physiology 417, 307322CrossRefGoogle ScholarPubMed
Yazejian, B.E., Cohen, B.N. & Fain, G.L. (1990). Acetylcholine (ACh) induces inward currents in isolated ganglion cells from the goldfish retina. Investigative Ophthalmology and Visual Science (ARVO Suppl.) 31, 389.Google Scholar
Yazejian, B. & Fain, G. (1991). Characterization of nicotinic acetylcholine receptors on isolated goldfish retinal ganglion cells. Society for Neuroscience Abstracts 17, Pt. 1, p. 343.Google Scholar
Yazejian, B. & Fain, G.L. (1992). Excitatory amino acid receptors on isolated retinal ganglion cells from the goldfish. Journal of Neurophysiology 67, 94107CrossRefGoogle ScholarPubMed
Zhang, Z.W. & Feltz, P. (1990). Nicotinic acetylcholine receptors in porcine hypophyseal intermediate lobe cells. Journal of Physiology 422, 83101CrossRefGoogle ScholarPubMed