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Temporal dynamics of contrast gain in single cells of the cat striate cortex

Published online by Cambridge University Press:  02 June 2009

A.B. Bonds
Affiliation:
Department of Electrical Engineering, Vanderbilt University, Nashville

Abstract

The response amplitude of cat striate cortical cells is usually reduced after exposure to high-contrast stimuli. The temporal characteristics and contrast sensitivity of this phenomenon were explored by stimulating cortical cells with drifting gratings in which contrast sequentially incremented and decremented in stepwise fashion over time. All responses showed a clear hysteresis, in which contrast gain dropped on average 0.36 log unit and then returned to baseline values within 60 s. Noticeable gain adjustments were seen in as little as 3 s and with peak contrasts as low as 3%. Contrast adaptation was absent in responses from LGN cells. Adaptation was found to depend on temporal frequency of stimulation, with greater and more rapid adaptation at higher temporal frequencies. Two different tests showed that the mechanism controlling response reduction was influenced primarily by stimulus contrast rather than response amplitude. These results support the existence of a rapid and sensitive cortically based system that normalizes the output of cortical cells as a function of local mean contrast. Control of the adaptation appears to arise at least in part across a population of cells, which is consistent with the idea that the gain control serves to limit the information converging from many cells onto subsequent processing areas.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

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References

Albrecht, D.G. & Hamilton, D.B. (1982). Striate cortex of monkey and cat: contrast response functions. Journal of Neurophysiology 48, 217237.Google Scholar
Albrecht, D.G., Farrar, S.B. & Hamilton, D.B. (1984). Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. Journal of Physiology 347, 713739.Google Scholar
Bauman, L.A. & Bonds, A.B. (1991). Inhibitory refinement of spatial-frequency selectivity in single cells of the cat striate cortex. Vision Research (in press).Google Scholar
Berkley, M.A. (1990). Behavioral determination of the spatial selectivity of contrast adaptation in cats: some evidence for a common plan in the mammalian visual system. Visual Neuroscience 4, 413426.Google Scholar
Blakemore, C.B. & Campbell, F.W. (1969). On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. Journal of Physiology 203, 237260.Google Scholar
Bonds, A.B. (1989). The role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Visual Neuroscience 2, 4155.Google Scholar
Dean, A.F. (1981). The relationship between response amplitude and contrast for cat striate cortical neurones. Journal of Physiology 318, 413427.Google Scholar
DeBruyn, E.J. & Bonds, A.B. (1986). Contrast adaptation in the cat is not mediated by GABA. Brain Research 383, 339342.Google Scholar
DeValois, K.K. & Tootell, R.B. (1983). Spatial-frequency-specific inhibition in cat striate cortical cells. Journal of Physiology 336, 359376.Google Scholar
Enroth-Cugell, C. & Shapley, R.M. (1973). Adaptation and dynamics of cat retinal ganglion cells. Journal of Physiology 233, 271309.Google Scholar
Garey, L.J. & Powell, T.P.S. (1971). An experimental study of the termination of the lateral geniculo-cortical pathway in cat and monkey. Proceedings of the Royal Society B (London) 179, 4163.Google Scholar
Hata, Y., Tsumoto, T., Hagihara, K. & Tamura, H. (1988). Inhibition contributes to Orientation selectivity in the cat. Nature 335, 815817.Google Scholar
Henry, G.H., Bishop, P.O., Tupper, R.M. & Dreher, B. (1973). Orientation specificity and response variability of cells in the striate cortex. Vision Research 13, 17711779.Google Scholar
Johnston, A. & Wright, M.J. (1983). Visual motion and cortical velocity. Nature 304, 436438.Google Scholar
Kaplan, E., Marcus, S. & So, Y.T. (1979). Effects of dark adaptation on spatial and temporal properties of receptive fields in cat lateral geniculate nucleus. Journal of Physiology 294, 561580.Google Scholar
Li, C.-Y. & Creutzfeldt, O.D. (1984). The representation of contrast and other stimulus parameters by single neurons in area 17 of the cat. Pflögers Archives 401, 304314.Google Scholar
Lorenceau, J. (1987). Recovery from contrast adaptation: effects of spatial and temporal frequency. Vision Research 27, 21852191.Google Scholar
Maddess, T., McCourt, M.E., Blakeslee, B. & Cunningham, R.B. (1988). Factors governing the adaptation of cells in area 17 of the cat visual cortex. Biological Cybernetics 59, 229236.Google Scholar
Magnussen, S. & Greenlee, M.W. (1985). Marathon adaptation to spatial contrast: saturation in sight. Vision Research 25, 14091411.Google Scholar
Matin, E. (1974). Light adaptation and the dynamics of induced tilt. Vision Research 14, 255265.Google Scholar
Morrone, M.C., Burr, D.C. & Maffei, L. (1982). Functional implications of cross-orientation inhibition of cortical visual cells. Proceedings of the Royal Society B 216, 335354.Google Scholar
Morrone, M.C., Burr, D.C. & Speed, H.D. (1987). Cross-orientation inhibition in cat is GABA mediated. Experimental Brain Research 67, 635644.Google Scholar
Movshon, J.A. & Lennie, P. (1979). Pattern-selective adaptation in visual cortical neurones. Nature 278, 850852.Google Scholar
Nelson, J.I., Seiple, W.H., Kupersmith, M.J. & Carr, R.E. (1984). A rapid evoked potential index of cortical adaptation. Electroencephalography and Clinical Neurophysiology 59, 454464.Google Scholar
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat's visual system. Journal of Neurophysiology 54, 651667.Google Scholar
Pantle, A. (1974). Motion aftereffect magnitude as a measure of the spatio-temporal response properties of direction-sensitive analyzers. Vision Research 14, 12291236.Google Scholar
Robson, J.G. (1975). Receptive fields: spatial and intensive representation of the visual image. In Handbook of Perception: Vision, ed. Carterette, D. & Friedman, W., pp. 81112. New York: Academic Press.Google Scholar
Sclar, G. & Freeman, R.D. (1982). Orientation selectivity in the cat's striate cortex is invarient with stimulus contrast. Experimental Brain Research 46, 457461.Google Scholar
Sclar, G., Lennie, P. & DePriest, D. (1989). Contrast adaptation in striate cortex of macaque. Vision Research 29, 747756.Google Scholar
Segundo, J.P. & Bell, C.C. (1970). Habituation of single nerve cells in the vertebrate nervous system. In Short-Term Changes in Neural Activity and Behavior, ed. Horn, G. & Hinde, R.N., pp. 7794. Cambridge: Cambridge University Press.Google Scholar
Skottun, B., DeValois, R.L., Grosof, D.H., Movshon, J.A., Al-Brecht, D.G. & Bonds, A.B. (1991). On classifying simple and complex cells according to response modulation. Vision Research (in press).Google Scholar
Sillito, A.M. (1975). The contribution of inhibitory mechanisms to the receptive-field properties of neurones in the striate cortex of the cat. Journal of Physiology 250, 305329.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
T'so, D.Y., Gilbert, C.D. & Wiesel, T.N. (1986). Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. Journal of Neuroscience 6, 11601170.Google Scholar
Vautin, R.G. & Berkley, M.A. (1978). Responses of single cells in cat visual cortex to prolonged stimulus movement: neural correlates of visual aftereffects. Journal of Neurophysiology 40, 10511065.Google Scholar
Vidyasagar, T.R. (1990). Pattern adaptation in cat visual cortex is a cooperative phenomenon. Neuroscience 36, 175179.Google Scholar
Wilson, H.R. (1990). Psychophysics of contrast gain control. Investigative Ophthalmology and Visual Science (Suppl.) 31, 430.Google Scholar