Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-06T10:14:32.419Z Has data issue: false hasContentIssue false

Substance P modulates calcium current in retinal bipolar neurons

Published online by Cambridge University Press:  02 June 2009

George S. Ayoub
Affiliation:
Department of Neurobiology and Behavior, The State University of New York, Stony Brook
Gary Matthews
Affiliation:
Department of Neurobiology and Behavior, The State University of New York, Stony Brook

Abstract

Retinal bipolar cells are non-spiking interneurons that relay information from photoreceptors to amacrine and ganglion cells. In turn, bipolar cells receive extensive synaptic feedback from amacrine cells, some of which contain neuropeptides, including substance P. We have examined the effect of substance P on single bipolar neurons isolated from goldfish retina and find that substance P (0.1–1 nM) produced a voltage-dependent inhibition of calcium current in these cells. The inhibition was strongest at negative potentials, with the peak suppression occurring at –20 to –30 mV; at potentials positive to 0 mV, there was little effect on calcium current. Thus, the net effect was to shift the voltage range of activation of calcium current toward more positive potentials. The inhibition of calcium current by substance P required GTP in the patch pipette and was blocked by internal GDP-β-S. Similar effects on calcium current were observed with somatostatin and metenkephalin, which are also found in amacrine cells.

Type
Research Articles
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

Bean, B.P. (1989). Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature 340, 153156.CrossRefGoogle ScholarPubMed
Bley, K.R. & Tsien, R.W. (1990). Inhibition of Ca2+ and K+ channels in sympathetic neurons by neuropeptides and other ganglionic transmitters. Neuron 2, 379391.CrossRefGoogle Scholar
Brecha, N., Sharma, S.C. & Karten, H.J. (1981). Localization of substance P-like immunoreactivity in the adult and developing goldfish retina. Neuroscience 6, 27372746.CrossRefGoogle ScholarPubMed
Djamooz, M.B.A., Downing, J.E.G. & Prince, D.J. (1983). Physiology of neuroactive peptides in vertebrate retina. Biochemical Society Transactions 11, 686689.CrossRefGoogle Scholar
Dolphin, A.C. (1990). G protein modulation of calcium currents in neurons. Annual Review of Physiology 52, 243255.CrossRefGoogle ScholarPubMed
Eskay, R.L., Long, R.T. & Iuvone, P.M. (1980). Evidence that TRH, somatostatin and substance P are present in neurosecretory elements of the vertebrate retina. Brain Research 196, 554559.CrossRefGoogle ScholarPubMed
Eskay, R.L., Furness, J.F. & Long, R.T. (1981). Substance P activity in the bullfrog retina: Localization and identification in several vertebrate species. Science 212, 10491051.CrossRefGoogle ScholarPubMed
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, 8199.CrossRefGoogle ScholarPubMed
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 Archiv 391, 85100.CrossRefGoogle ScholarPubMed
Heidelberger, R. & Matthews, G. (1991). Inhibition of calcium influx and calcium current by γ-aminobutyric acid in single synaptic terminals. Proceedings of the National Academy of Sciences of the U.S.A. 88, 71357139.CrossRefGoogle ScholarPubMed
Heidelberger, R. & Matthews, G. (1992). Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. Journal of Physiology (in press).CrossRefGoogle ScholarPubMed
Ishida, A.T., Stell, W.K. & Lightfoot, D.O. (1980). Rod and cone inputs to bipolar cells in goldfish retina. Journal of Comparative Neurology 191, 315335.CrossRefGoogle ScholarPubMed
Lasater, E.M., Watling, K.J. & Dowling, J.E. (1983). Vasoactive intestinal peptide alters membrane potential and cyclic nucleotide levels in retinal horizontal cells. Science 224, 10701072.CrossRefGoogle Scholar
Li, H.-B., Marshak, S.W., Dowling, J.E. & Lam, D.M.-K. (1986). Colocalization of immunoreactive substance P and neurotensin in araacrine cells of the goldfish retina. Brain Research 336, 307313.Google Scholar
Maggio, J.E. (1988). Tachykinins. Annual Review of Neuroscience 11, 1328.CrossRefGoogle ScholarPubMed
Marshak, D.W. (1992). Peptidergic neurons of teleost retinas. Visual Neuroscience 8, 137144.CrossRefGoogle ScholarPubMed
Nicoll, R.A., Schenker, C. & Leeman, S.E. (1980). Substance P as a neurotransmitter candidate. Annual Review of Neuroscience 3, 227268.CrossRefGoogle Scholar
Saito, T., Kujiraoka, T. & Yonaha, T. (1983). Connections between photoreceptors and horseradish peroxidase-injected bipolar cells in the carp retina. Vision Research 23, 353362.CrossRefGoogle ScholarPubMed
Stanfield, P.R., Nakajima, Y. & Yamaguchi, K. (1985). Substance P raises neuronal membrane excitability by reducing inward rectification. Nature 315, 498501.CrossRefGoogle ScholarPubMed
Stell, W.K. (1985). Putative peptide transmitters, amacrine cell diversity and function in the inner plexiform layer. In Neurocircuitry of the Retina, A Cajal Memorial, ed. Gallego, A. & Gouras, P., pp. 171187. New York: Elsevier Science Publishing Co., Inc.Google Scholar
Tachibana, M. (1983). Ionic currents of solitary horizontal cells isolated from goldfish retina. Journal of Physiology 345, 329351.CrossRefGoogle ScholarPubMed
Yamaguchi, K., Nakajima, Y., Nakajima, S. & Stanfield, P.R. (1990). Modulation of inwardly rectifying channels by substance P in cholinergic neurones from rat brain in culture. Journal of Physiology 426, 499520.CrossRefGoogle ScholarPubMed
Yazulla, S., Studholme, K.M. & Zucker, C.L. (1985). Synaptic organization of substance P-like immunoreactive amacrine cells in goldfish retina. Journal of Comparative Neurology 231, 232238.CrossRefGoogle ScholarPubMed
Zalutsky, R.A. & Miller, R.F. (1990). The physiology of substance P in the rabbit retina. Journal of Neuroscience 10, 394402.CrossRefGoogle ScholarPubMed