Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T07:59:13.516Z Has data issue: false hasContentIssue false

Variability in the firing of retinal ganglion cells of goldfish: A review

Published online by Cambridge University Press:  29 May 2007

MICHAEL W. LEVINE
Affiliation:
Department of Psychology and Laboratory for Integrative Neuroscience, University of Illinois at Chicago, Chicago, Illinois

Abstract

The isolated retina of the goldfish has proven a valuable resource for studying the variability of firing of retinal ganglion cells. Three major areas of study are considered here: the variability of maintained discharges, the correlated firing of neighboring ganglion cells, and the variability of responses to light. The sources of variability, its relationship to retinal processing, and its possible functional role in perception are examined through these three aspects of variability. The results are related to similar studies in mammals (mainly cats). This retrospective is biased toward my studies over 30 years.

Type
REVIEW ARTICLE
Copyright
© 2007 Cambridge University Press

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

REFERENCES

Ariel, M. & Daw, N.W. (1982). Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. Journal of Physiology 324, 135160.CrossRefGoogle Scholar
Arnett, D.W. (1978). Statistical dependence between neighboring retinal ganglion cells in goldfish. Experimental Brain Research 32, 4953.Google Scholar
Bilotta, J. & Abramov, I. (1989). Spatial properties of goldfish ganglion cells. Journal of General Physiology 93, 11471169.CrossRefGoogle Scholar
Chapman, R.M., McCrary, J.W. & Tuttle, J.R. (1981). Principal components analysis of sources of variability in retinal ganglion cell responses. Biological Cybernetics 42, 4550.CrossRefGoogle Scholar
Dean, A.F. (1981). The variability of discharge of simple cells in the cat striate cortex. Experimental Brain Research 44, 437440.Google Scholar
Dowling, J.E. (1979). A new retinal neurone—the interplexiform cell. Trends in Neuroscience 2, 189191.CrossRefGoogle Scholar
Dubin, M.W. (1970). The inner plexiform layer of the vertebrate retina: A quantitative and comparative electron microscopic analysis. Journal of Comparative Neurology 140, 479506.CrossRefGoogle Scholar
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517552.CrossRefGoogle Scholar
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193195.CrossRefGoogle Scholar
Frishman, L.J. & Levine, M.W. (1983). Statistics of the maintained discharge of cat retinal ganglion cells. Journal of Physiology 339, 475494.CrossRefGoogle Scholar
Ginsburg, K.S., Johnsen, J.A. & Levine, M.W. (1984). Common noise in the firing of neighbouring ganglion cells in goldfish retina. Journal of Physiology 351, 433450.CrossRefGoogle Scholar
Gray, C.M. & Singer, W. (1989). Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proceedings of the National Academy of Sciences 86, 16981702.CrossRefGoogle Scholar
Johnsen, J.A. & Levine, M.W. (1983). Correlation of activity in neighbouring goldfish ganglion cells: Relationship between latency and lag. Journal of Physiology 345, 439449.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
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 3768.Google Scholar
Levine, M.W. (1980). Firing rates of a retinal neuron are not predictable from interspike interval statistics. Biophysical Journal 30, 926.CrossRefGoogle Scholar
Levine, M.W. (1982). Retinal processing of intrinsic and extrinsic noise. Journal of Neurophysiology 48, 9921010.Google 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 Scholar
Levine, M.W. (1997). An analysis of the cross-correlation between ganglion cells in the retina of goldfish. Visual Neuroscience 14, 731739.CrossRefGoogle Scholar
Levine, M.W. (2004). The potential coding utility of intercell cross-correlations in the retina. Biological Cybernetics 91, 182187.Google Scholar
Levine, M.W., Castaldo, K. & Kasapoglu, M.B. (2002). Firing coincidences between neighboring retinal ganglion cells: Inside information or epiphenomenon? BioSystems 67, 139146.Google Scholar
Levine, M.W., Cleland, B.G., Mukherjee, P. & Kaplan, E. (1996). Tailoring of variability in the lateral geniculate nucleus of the cat. Biological Cybernetics 75, 219227.CrossRefGoogle Scholar
Levine, M.W., Cleland, B.G. & Zimmerman, R.P. (1992). Variability of responses of cat retinal ganglion cells. Visual Neuroscience 8, 277279.CrossRefGoogle Scholar
Levine, M.W. & Shefner, J.M. (1975). Independence of “on” and “off” responses of retinal ganglion cells. Science 190, 12151217.CrossRefGoogle Scholar
Levine, M.W. & Shefner, J.M. (1977a). A model for the variability of interspike intervals during sustained firing of a retinal neuron. Biophysical Journal 19, 241252.Google Scholar
Levine, M.W. & Shefner, J.M. (1977b). Variability in ganglion cell firing patterns: Implications for separate “on” and “off” processes. Vision Research 17, 765776.Google Scholar
Levine, M.W. & Shefner, J.M. (1979). X-like and not X-like cells in goldfish retina. Vision Research 19, 9597.CrossRefGoogle Scholar
Levine, M.W. & Zimmerman, R.P. (1991). A model for the variability of maintained discharges and responses to flashes of light. Biological Cybernetics 65, 469477.CrossRefGoogle Scholar
Levine, M.W., Saleh, E.J. & Yarnold, P.R. (1988a). Statistical properties of the maintained discharge of chemically isolated ganglion cells in goldfish retina. Visual Neuroscience 1, 3146.Google Scholar
Levine, M.W., Zimmerman, R.P. & Carrión-Carire, V. (1988b). Variability in responses of retinal ganglion cells. Journal of the Optical Society of America A 5, 593597.Google Scholar
MacNichol, E.F., Jr. & Svaetichin, G. (1958). Electric responses from the isolated retinas of fishes. American Journal of Ophthalmology 46, 2640.CrossRefGoogle Scholar
Mastronarde, D.N. (1983a). Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. Journal of Neurophysiology 49, 303324.Google Scholar
Mastronarde, D.N. (1983b). Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. Journal of Neurophysiology 49, 325349.Google Scholar
Mastronarde, D.N. (1983c). Interactions between ganglion cells in cat retina. Journal of Neurophysiology 49, 350365.Google Scholar
Meister, M. (1996). Multineuronal codes in retinal signaling. Proceedings of the American Academy of Sciences 93, 609614.CrossRefGoogle Scholar
Meister, M.M., Lagnado, L. & Baylor, D.A. (1995). Concerted signaling by retinal ganglion cells. Science 270, 12071210.CrossRefGoogle Scholar
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
Nirenberg, S., Carcieri, S.M., Jacobs, A.L. & Latham, P.E. (2001). Retinal ganglion cells act largely as independent encoders. Nature 411, 698701.CrossRefGoogle Scholar
Samonds, J.M., Allison, J.D., Brown, H.A. & Bonds, A.B. (2004). Cooperative synchronized assemblies enhance orientation discrimination. Proceedings of the National Academy of Sciences 101, 67226727.CrossRefGoogle Scholar
Samonds, J.M. & Bonds, A.B. (2004). From another angle: Differences in cortical coding between fine and coarse discrimination of orientation Journal of Neurophysiology 91, 11931202.Google Scholar
Schellart, N.A.M. & Spekreijse, H. (1973). Origin of the stochastic nature of ganglion cell activity in isolated goldfish retina. Vision Research 13, 337345.CrossRefGoogle Scholar
Shapley, R.M. & Victor, J.D. (1981). How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. Journal of Physiology 318, 161179.CrossRefGoogle Scholar
Shefner, J.M. & Levine, M.W. (1979). An analysis of receptor inputs to and spatial distribution of ganglion cell on and off processes. Vision Research 19, 647653.CrossRefGoogle Scholar
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149185.CrossRefGoogle Scholar
Stevens, C.F. & Zador, A.M. (1998). Input synchrony and the irregular firing of cortical neurons Nature Neuroscience 1, 210217.Google Scholar
Stone, J. & Hoffmann, K.-P. (1972). Very slow-conducting ganglion cells in the cat's retina: A major, new functional type? Brain Research 43, 610616.Google Scholar
Tolhurst, D.J., Movshon, J.A. & Dean, A.F. (1983). The statistical reliability of signals in single neurons in cat and monkey visual cortex, Vision Research 23, 775785.Google Scholar
Tolhurst, D.J., Movshon, J.A. & Thompson, I.D. (1981). The dependence of response amplitude and variance of cat visual cortical neurones on stimulus contrast. Experimental Brain Research 41, 414419.Google Scholar
Toyoda, J.-I. (1974). Frequency characteristics of retinal neurons in the carp. Journal of General Physiology 63, 214234.CrossRefGoogle Scholar
Toyoda, J., Shimbo, K., Kondo, H. & Kujiraoka, T. (1992). Push-pull modulation of ganglion cell responses in carp retina by amacrine cells. Neuroscience Letters 142, 4144.CrossRefGoogle Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447480.Google Scholar
Weakly, J.N. (1973). The action of cobalt ions on neuromuscular transmission in the frog. Journal of Physiology 234, 597612.CrossRefGoogle Scholar