Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-25T05:04:55.042Z Has data issue: false hasContentIssue false

Statistical properties of the maintained discharge of chemically isolated ganglion cells in goldfish retina

Published online by Cambridge University Press:  02 June 2009

Michael W. Levine
Affiliation:
Department of Psychology
Edward J. Saleh
Affiliation:
The Committee on Neuroscience
Paul R. Yarnold
Affiliation:
University of Illinois at Chicago, Chicago

Abstract

Action potentials were recorded from isolated goldfish retinae maintained in a superfusate of Ringer's solution. Responses to flashes of light and maintained discharges were obtained from 84 cells. The properties of these cells were compared to those in two other goldfish preparations: the isolated retina maintained in a flow of moist oxygen and the self-respiring fish. Maintained discharges of cells in the superfused retinae tended to have lower mean firing rates, higher variability, and weaker high-pass properties than had been observed in the previous preparations. These properties seemed insensitive to the particular formulae used to superfuse the retinae.

Cobalt, which disables synapses, dramatically reduced maintained firing and eliminated photic responses. Cells that did fire in the presence of cobalt generally had low variabilities before cobalt was added; their firing in cobalt was considerably more variable than the baseline. Nevertheless, cobalt did not seem to change the temporal dependency (high-pass properties) of the maintained discharges. The cholinergic agonist carbachol had an excitatory effect upon 71% of the cells tested. Bursty or oscillatory firing in cobalt was rendered more regular by the addition of carbachol. With the exception of the mean firing rate, none of the statistical properties of the maintained discharge differed in cobalt plus carbachol from those in normal Ringer's solution.

There was a tendency for the statistical properties of the maintained discharge after the treatment to approach those of the previously reported preparations; the treatment was at least partially responsible for the drift in properties. The results are discussed in terms of the possible sources of variability in the ganglion cell's discharge, with particular reference to the high-pass filter that appears to act upon it.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1988

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

Abramov, I. & Levine, M.W. (1972). The effects of carbon dioxide on the excised goldfish retina. Vision Research 12, 18811895.CrossRefGoogle ScholarPubMed
Ayoub, G.S. & Lam, D.M.-K. (1984). The release of Ϝ–aminobutyric acid from horizontal cells of the goldfish (Carassius auratus) retina. Journal of Physiology 355, 191214.CrossRefGoogle ScholarPubMed
Belgum, J.H, Dvorak, D.R., McReynolds, J.S. (1983). Sustained and transient synaptic inputs to on-off ganglion cells in the mudpuppy retina. Journal of Physiology 340, 599610.CrossRefGoogle ScholarPubMed
Bourhim, N., Castanas, E., Giraud, P., Cantau, P. & Oliver, C. (1985). Modification of opioid ligand binding in the central and the peripheral nervous system by different buffers. Biochemical and Biophysical Research Communications 129, 328333.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Miller, R.F. (1976). Photoreceptor-bipolar cell transmission in the perfused retina eyecup of the mudpuppy. Science 191, 963964.CrossRefGoogle ScholarPubMed
Dacheux, R.F., Frumkes, T.E. & Miller, R.F. (1979). Pathways and polarities of synaptic interactions in the inner retina of the mudpuppy, 1: Synaptic blocking studies. Brain Research 161, 112.CrossRefGoogle ScholarPubMed
Davidoff, R.A. & Sears, E.S. (1975). Effects of synthetic buffers on reflexes in the isolated frog spinal cord. American Journal of Physiology 229, 831837.CrossRefGoogle ScholarPubMed
Van Duk, B.W. & Ringo, J.L. (1987). The variation in the light responses of carp retinal ganglion cells is independent of response amplitude. Vision Research 27, 493497.CrossRefGoogle Scholar
Evans, J.A., Hood, D.C. & Holtzman, E. (1978). Differential effects of cobalt ions on rod and cone synaptic activity in the isolated frog retina. Vision Research 18, 145151.CrossRefGoogle ScholarPubMed
Frishman, L.J. & Levine, M.W. (1983). Statistics of the maintained discharge of cat retinal ganglion cells. Journal of Physiology 339, 475494.CrossRefGoogle ScholarPubMed
Gillespie, J.S. & McKnight, A.T. (1976). Adverse effects of Tris hydrochloride, a commonly used buffer in physiological media. Journal of Physiology 259, 561573.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
Good, N.E., Winget, G.D., Winter, W., Connolly, T.N., Izawa, S., & Singh, R.M.M. (1966). Hydrogen ion buffers for biological research. Biochemistry 5, 467477.CrossRefGoogle ScholarPubMed
Green, P.E. (1978). Analyzing Multivariate Data. Hinsdale, Illinois: Dryden Press.Google Scholar
Hartline, H.K. (1938). The response of single optic nerve fibers of the vertebrate eye to illumination of the retina. American Journal of Physiology 121, 400415.CrossRefGoogle Scholar
Kato, S., Sugawara, K. & Negishi, K. (1983). Light-evoked and antidromic activation of ganglion cells of the carp retina in a chloride free medium. Vision Research 23, 17451747.CrossRefGoogle Scholar
Kondo, H. & Toyoda, J.-I. (1983). GABA and glycine effects on the bipolar cells of the carp retina. Vision Research 23, 12591264.CrossRefGoogle ScholarPubMed
Lasater, E.M. & Lam, D.M.K. (1984). The identification and some functions of GABAergic neurons in the distal catfish retina. Vision Research 24, 497506.CrossRefGoogle ScholarPubMed
Levine, M.W. (1980 a). Maintained discharge of ganglion cells, the tabula rasa for sensory signals. Investigative Ophthalmology and Visual Science 19 (supplement), 6.Google Scholar
Levtne, M.W. (1980 b). Firing rates of a retinal neuron are not predictable from interspike interval statistics. Biophysical Journal 30, 926.Google Scholar
Levine, M.W. (1982). Retinal processing of intrinsic and extrinsic noise. Journal of Neurophysiology 48, 9921010.CrossRefGoogle Scholar
Levine, M.W. (1987). Variability in the maintained discharges of retinal ganglion cells. Journal of the Optical Society of America A 4, 23082320.CrossRefGoogle ScholarPubMed
Levine, M.W. & Saleh, E.J. (1984). Processes and mechanisms controlling the firing of retinal ganglion cells in the goldfish. Investigative Ophthalmology and Visual Science 25 (supplement), 119.Google Scholar
Levine, M.W. & Shefner, J.M. (1977 a). Variability in ganglion cell firing patterns: implications for separate “on” and “off” processes. Vision Research 17, 765776.CrossRefGoogle Scholar
Levine, M.W. & Shefner, J.M. (1977 b). A model for the variability of interspike intervals during sustained firing of a retinal neuron. Biophysical Journal 19, 241252.CrossRefGoogle Scholar
Levtne, M.W. & Shefner, J.M. (1979). X-like and not-X-like cells in goldfish retina. Vision Research 19, 9597.Google Scholar
Levine, M.W. & Shefner, J.M. (1981). Distance-dependent interactions between the rod and the cone systems in goldfish retina. Experimental Brain Research 44, 353361.CrossRefGoogle ScholarPubMed
Llinas, R. & Jahnsen, H. (1982). Electrophysiology of mammalian thalamic neurones in vitro. Nature 297, 406408.CrossRefGoogle ScholarPubMed
Masland, R.H. & Ames, A. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 12201235.CrossRefGoogle Scholar
Miller, R.F., Frumkes, T.E., Slaughter, M. & Dacheux, R.F. (1981). Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina, II: Amacrine and ganglion cells. Journal of Neurophysiology 45, 764782.CrossRefGoogle ScholarPubMed
Miller, A.M. & Schwartz, E.A. (1983). Evidence for the identification of synaptic transmitters released by photoreceptors of the toad retina. Journal of Physiology 334, 325349.CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S., Teranishi, T. & Laufer, M. (1978). An electrophysiological study on the cholinergic system in the carp retina. Brain Research 148, 8593.CrossRefGoogle Scholar
Schellart, N.A.M. & Spekreuse, H. (1973). Origin of the stochastic nature of ganglion cell activity in isolated goldfish retina. Vision Research 13, 337345.CrossRefGoogle ScholarPubMed
Schwartz, E.A. (1982). Calcium-independent release of GABA from isolated horizontal cells of the toad retina. Journal of Physiology 323, 211227.CrossRefGoogle ScholarPubMed
Shefner, J.M. & Levine, M.W. (1976). A method for obtaining single cell responses in the optic tract of self-respiring fish. Behavioral Research Methods and Instrumentation 8, 453455.CrossRefGoogle Scholar
Shefner, J.M. & Levine, M.W. (1979). A comparison of properties of goldfish retinal ganglion cells as a function of lighting conditions during dissection. Vision Research 19, 8389.CrossRefGoogle ScholarPubMed
Weakly, J.N. (1973). The action of cobalt ions on neuromuscular transmission in the frog. Journal of Physiology 234, 597612.CrossRefGoogle ScholarPubMed
Wolbarsht, M.L. & Wagner, H.G. (1963). Glass-insulated platinum microelectrodes: design and fabrication. In Medical Electronics, ed. Bostem, H., pp. 510515. Liege: University of Liege Press.Google Scholar
Wu, S.M. & Dowling, J.E. (1978). L-aspartate: evidence for a role in cone photoreceptor synaptic transmission in the carp retina. Proceedings of the National Academy of Sciences 75, 52055209.CrossRefGoogle ScholarPubMed
Yazulla, S. (1983). Stimulation of GABA release from horizontal cells by potassium and acidic amino acid agonists. Brain Research 275, 6174.CrossRefGoogle ScholarPubMed