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Conductances evoked by light in the ON-β ganglion cell of cat retina

Published online by Cambridge University Press:  02 June 2009

Michael A. Freed
Affiliation:
Laboratory of Neurophysiology, National Institute of Neurological Disorders and Stroke, Bethesda
Ralph Nelson
Affiliation:
Laboratory of Neurophysiology, National Institute of Neurological Disorders and Stroke, Bethesda

Abstract

When a bar of light (215 x 5000 μm) illuminates the receptive field of an ON-β ganglion cell of cat retina, the cell depolarizes. Intracellular recording from the cat eyecup preparation shows that this depolarization is due to an increase in conductance (2.4 ± 0.6 nS). Different phases of this depolarization have different reversal potentials, but all of these reversal potentials are more positive than the cell’s resting potential in the dark. When the light is turned on, there is an initial transient depolarization; the reversal potential measured for this transient is positive (23 ± 11 mV). As the light is left on, the cell partially repolarizes to a sustained depolarization; the reversal potential measured for this sustained depolarization is close to zero (−1 ± 5 mV). When the light is turned off, the cell repolarizes further; the reversal potential measured for this repolarization is negative (−18 ± 7 mV), but still above the resting potential in the dark (−50 mV). To explain this variety of reversal potentials, at least two different synaptic conductances are required: one to ions which have a positive reversal potential and another to ions which have a negative reversal potential. Comparing the responses to broad and narrow bars suggests that these two conductances are associated with the center and surround, respectively. Finally, since an ON-β cell in the area centralis receives about 200 synapses, these results indicate that a single synapse produces an average conductance increase of about 15 pS during a near-maximal depolarization.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

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References

Arkin, M.S. & Miller, R.F. (1988). Synaptic inputs and morphology of sustained ON-ganglion cells in the mudpuppy retina. Journal of Neurophysiology 60, 11431159.CrossRefGoogle ScholarPubMed
Belgum, J.H., Dvorak, D.R. & McReynolds, J.S. (1982). Sustained synaptic input to ganglion cells of mudpuppy retina. Journal of Physiology (London) 326, 91108.CrossRefGoogle ScholarPubMed
Belgum, J.H., Dvorak, D.R., McReynolds, J.S. & Miyachi, E. (1987). Push-pull effect of surround illumination on excitatory and inhibitory inputs to mudpuppy retinal ganglion cells. Journal of Physiology (London) 388, 233243.CrossRefGoogle ScholarPubMed
Bishop, P.O., Kozak, W. & Vakkur, G.J. (1962). Some quantitative aspects of the cat’s eye: Axis and plane of reference, visual field coordinates, and optics. Journal of Physiology (London) 163, 466502.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat’s retina. Journal of Physiology (London) 240, 397419.CrossRefGoogle ScholarPubMed
Brown, J.E., Muller, K.J. & Murray, G. (1971). Reversal potential for an electrophysiological event generated by conductance changes: Mathematical analysis. Science 174, 318.CrossRefGoogle ScholarPubMed
Cleland, B.G., Harding, T.H. & TULUNAY-Keesey, U. (1979). Visual resolution and receptive field size: Examination of two kinds of cat retinal ganglion cell. Science 205, 10151017.CrossRefGoogle ScholarPubMed
Cohen, E. & Sterling, P. (1986). Accumulation of (3H)glycine by cone bipolar cells in the cat retina. Journal of Comparative Neurology 250, 17.CrossRefGoogle ScholarPubMed
Cohen, E. & Sterling, P. (1991). Microcircuitry related to the receptive-fīeld center of the ON-beta ganglion cell. Journal of Neurophysiology 65, 352359.CrossRefGoogle Scholar
Coleman, P.A. & Miller, R.F. (1989). Measurement of passive membrane parameters with whole-cell recording from neurons in the intact amphibian retina. Journal of Neurophysiology 61, 218230.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology (London) 187, 517552.CrossRefGoogle ScholarPubMed
Freed, M.A. & Nelson, R. (1993). Noise analysis of ON-β ganglion cell voltage responses. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1154.Google Scholar
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 23032320.CrossRefGoogle ScholarPubMed
Freed, M.A., Smith, R.G. & Sterling, P. (1992). Computational model of the ON-alpha ganglion cell receptive field based on bipolar cell circuitry. Proceeding of the National Academy of Sciences of the U.S.A. 89, 236240.CrossRefGoogle ScholarPubMed
Gaudiano, P. (1992). A unified neural network model of spatiotemporal processing in X and Y retinal ganglion cells: I: Analytical results. Biological Cybernetics 67, 1121.CrossRefGoogle Scholar
Hille, B. (1984). Ionic Channels of Excitable Membranes. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 3768.CrossRefGoogle ScholarPubMed
Linsenmeier, R.A., Frishman, L.J., Jakiela, H.G. & Enroth-Cugell, C. (1982). Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements. Vision Research 22, 11731183.CrossRefGoogle ScholarPubMed
Lipton, S.A. & Tauck, D.L. (1987). Voltage-dependent conductances of solitary ganglion cells dissociated from the rat retina. Journal of Physiology (London) 385, 361391.CrossRefGoogle ScholarPubMed
Mcguire, B.A., Stevens, J.K. & Sterling, P. (1986). Microcircuitry of beta ganglion cells in cat retina. Journal of Neuroscience 6, 907918.CrossRefGoogle ScholarPubMed
Meyer, S.L. (1975). Data Analysis for Scientists and Engineers. New York: Wiley.Google Scholar
Nelson, R. (1977). Cat cones have rod input: A comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. Journal of Comparative Neurology 172, 109135.CrossRefGoogle ScholarPubMed
Nelson, R., Famiglietti, E.V. Jr, & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for ON- and OFF- center ganglion cells in cat retina. Journal of Neurophysiology 41, 472483.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 11831195.CrossRefGoogle ScholarPubMed
Nelson, R., Kolb, H. & Freed, M.A. (1993). OFF-alpha and OFF-beta ganglion cells in cat retina. 1. Intracellular electrophysiology and HRP stains. Journal of Comparative Neurology 329, 6884.CrossRefGoogle ScholarPubMed
Press, W., Flannery, B., Teukolsky, S. & Vetterling, W. (1989). Numerical Recipes in Pascal. New York, New York: Cambridge University Press.Google Scholar
Saito, H. (1983). Pharmacological and morphological differences between X- and Y-type ganglion cells in the cat’s retina. Vision Research 23, 12991308.CrossRefGoogle ScholarPubMed
Smith, R.G. & Sterling, P. (1990). Cone receptive field in cat retina computed from microcircuitry. Visual Neuroscience 5, 453461.CrossRefGoogle ScholarPubMed
Staley, K.J., Otis, T.S. & Mody, I. (1992). Membrane properties of dentate gyrus granule cells: Comparison of sharp microelectrode and whole-cell recordings. Journal of Neurophysiology 67, 13461358.CrossRefGoogle ScholarPubMed
WÄSsle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447480.CrossRefGoogle ScholarPubMed
Wunk, D.F. & Werblin, F.S. (1979). Synaptic inputs to the ganglion cells in the tiger salamander retina. Journal of General Physiology 73, 265286.CrossRefGoogle Scholar
Zar, J.H. (1974). Biostatistical Analysis. Englewood Cliffs, New Jersey: Prentice-Hall, Inc.Google Scholar