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Role of Inhibition in the Specification of Orientation Selectivity of Cells in the Cat Striate Cortex

  • A. B. Bonds (a1)


Mechanisms supporting orientation selectivity of cat striate cortical cells were studied by stimulation with two superimposed sine-wave gratings of different orientations. One grating (base) generated a discharge of known amplitude which could be modified by the second grating (mask). Masks presented at nonoptimal orientations usually reduced the base-generated response, but the degree of reduction varied widely between cells. Cells with narrow orientation tuning tended to be more susceptible to mask presence than broadly tuned cells; similarly, simple cells generally showed more response reduction than did complex cells.

The base and mask stimuli were drifted at different temporal frequencies which, in simple cells, permitted the identification of individual response components from each stimulus. This revealed that the reduction of the base response by the mask usually did not vary regularly with mask orientation, although response facilitation from the mask was orientation selective. In some sharply tuned simple cells, response reduction had clear local maxima near the limits of the cell's orientation-tuning function.

Response reduction resulted from a nearly pure rightward shift of the response versus log contrast function. The lowest mask contrast yielding reduction was within 0.1–0.3 log unit of the lowest contrast effective for excitation.

The temporal-frequency bandpass of the response-reduction mechanism resembled that of most cortical cells. The spatial-frequency bandpass was much broader than is typical for single cortical cells, spanning essentially the entire visual range of the cat.

These findings are compatible with a model in which weak intrinsic orientation-selective excitation is enhanced in two stages: (1) control of threshold by nonorientation-selective inhibition that is continuously dependent on stimulus contrast; and (2) in the more narrowly tuned cells, orientation-selective inhibition that has local maxima serving to increase the slope of the orientation-tuning function.



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Albus, K. (1975). A quantitative study of the projection area of the central and paracentral visual field in the cat: the spatial organization in the orientation domain. Experimental Brain Research 24, 181202.
Albrecht, D.G., Farrar, S. & Hamilton, D.B. (1984). Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. Journal of Physiology 347, 713739.
Bishop, P.O., Coombs, J.S. & Henry, G.H. (1973). Receptive fields of simple cells in the cat striate cortex. Journal of Physiology 231, 3160.
Creutzfeldt, O.D. & Ito, M. (1968). Functional synaptic organization of primary visual cortex neurons in the cat. Experimental Brain Research 6, 324352.
Creutzfeldt, O.D., Innocenti, G.M. & Brooks, D. (1974 a). Vertical organization in the visual cortex (Area 17). Experimental Brain Research 21, 315336.
Creutzfeldt, O.D., Kuhnt, U. & Benevento, L.A. (1974 b). An intracellular analysis of visual cortical neurons to moving stimuli: responses in a cooperative neuronal network. Experimental Brain Research 21, 251274.
Dealy, R.S. & Tolhurst, D.J. (1974). Is spatial adaptation an after-effect of prolonged inhibition? Journal of Physiology 241, 261270.
DeBruyn, E.J. & Bonds, A.B. (1986). Contrast adaptation in cat visual cortex is not mediated by GABA. Brain Research 383, 339342.
DeBruyn, E.J., Gajewski, Y.A. & Bonds, A.B. (1986). Anti-cholinesterase agents affect the gain of the cat cortical VEP. Neuroscience Letters 71, 311317.
DeValois, K.K. & Tootell, R.B.H. (1983). Spatial-frequency-specific inhibition in cat striate cortex cells. Journal of Physiology 336, 359376.
Ferster, D. (1986). Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. Journal of Neuroscience 6, 12841301.
Ferster, D. & Lindstrom, S. (1983). An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat. Journal of Physiology 342, 181215.
Garey, L.J. (1971). A light and electron microscopic study of the visual cortex of the cat and monkey. Proceedings of the Royal Society B (London) 179, 2140.
Garey, L.J. & Powell, T.P.S. (1971). An experimental study of the termination of the lateral geniculo-cortical pathway in the cat. Proceedings of the Royal Society B (London) 179, 4163.
Gilbert, C.D. & Wiesel, T.N. (1979). Morphology and intracortical projections of functionally characterized neurones in the cat visual cortex. Nature 280, 120125.
Gilbert, C.D. & Wiesel, T.N. (1983). Clustered intrinsic connections in cat visual cortex. Journal of Neuroscience 3, 11161133.
Hammond, P. (1978). On the use of nitrous oxide/oxygen mixtures for anesthesia in cats. Journal of Physiology 275, 64P.
Heggelund, P. (1981 a). Receptive-field organization of simple cells in cat striate cortex. Experimental Brain Research 42, 8998.
Heggelund, P. (1981 b). Receptive-field organization of complex cells in cat striate cortex. Experimental Brain Research 42, 99107.
Henry, G.H., Bishop, P.O., Tupper, R.M. & Dreher, B. (1973). Orientation specificity of cells in cat striate cortex. Vision Research 13, 17711779.
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106154.
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.
Legge, G.E. & Foley, J.M. (1980). Contrast matching in human vision. Journal of the Optical Society of America 70, 14581471.
Lennie, P. (1980). Parallel visual pathways: a review. Vision Research 20, 561594.
LeVay, S. (1973). Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi preparations. Journal of Comparative Neurology 150, 5386.
Levick, W.R. (1972). Another tungsten microelectrode. Medical and Biological Engineering 10, 510515.
Levick, W.R. & Thibos, L.N. (1982). Analysis of orientation bias in cat retina. Journal of Physiology 329, 243261.
Li, C.Y. & Creutzfeldt, O.D. (1984). The representation of contrast and other stimulus parameters by single neurons in area 17 of the cat. Pflugers Archives 401, 304314.
Milkman, N., Shapley, R.M. & Schick, G. (1978). A microcomputer-based visual stimulator. Behavior Research Methods and Instrumentation 10, 539545.
Morrone, M.C., Burr, D.C. & Maffei, L. (1982). Functional implications of cross-orientation inhibition of cortical visual cells. Proceedings of the Royal Society of London (Biology) 216, 335354.
Movshon, J.A. & Lennie, P. (1979). Pattern-selective adaptation in visual cortical neurones. Nature 278, 850851.
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978 a). Spatial summation in the receptive fields of simple cells in the cat's striate cortex. Journal of Physiology 283, 5377.
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978 b). Receptive field organization of complex cells in the cat's striate cortex. Journal of Physiology 283, 7999.
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978 c). Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. Journal of Physiology 283, 101120.
Nelson, J.I. & Frost, B.J. (1978). Orientation-selective inhibition from beyond the classic visual receptive field. Brain Research 139, 359364.
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat visual system. Journal of Neurophysiology 54, 651665.
Orban, G.A. (1984). Neuronal Operations in the Visual Cortex. Berlin: Springer-Verlag.
Peters, A. & Fairen, A. (1978). Smooth and sparsely spined stellate cells in the visual cortex of the rat: a study using a combined Golgi-electron microscope technique. Journal of Comparative Neurology 181, 129172.
Pfleger, B., Bonds, A.B. & DeBruyn, E.J. (1987). The limited role of GABA in orientation tuning of visual cortical cells of the cat. Investigative Ophthalmology and Visual Science (Suppl.) 28, 198.
Ratliffe, F. (1965). Mach Bands: Quantitative Studies on Neural Networks in the Retina. San Francisco: Holden-Day.
Ribak, C.E. (1978). Aspinous and sparsely spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase. Journal of Neurocytology 7, 461478.
Sclar, G. & Freeman, R.D. (1982). Orientation selectivity in the cat's striate cortex is invariant with stimulus contrast. Experimental Brain Research 46, 457461.
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.
Sillito, A.M. (1977). Inhibitory processes underlying the directional specificity of simple, complex, and hypercomplex cells in the cat's visual cortex. Journal of Physiology 271, 699720.
Sillito, A.M. (1979). Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. Journal of Physiology 289, 3353.
Sillito, A.M., Kemp, J.A., Milson, J.A. & Berardi, N. (1980). A reevaluation of the mechanisms underlying simple cell orientation selectivity. Brain Research 194, 517520.
Soodak, R.E., Shapley, R.M. & Kaplan, E. (1987). Linear mechanism of orientation tuning in the retina and lateral geniculate of the cat. Journal of Neurophysiology 58, 267275.
Tanaka, K. (1985). Organization of geniculate inputs to visual cortical cells in the cat. Vision Research 25, 357364.
Tolhurst, D.J. & Movshon, J.A. (1975). Spatial and temporal contrast sensitivity of striate cortical neurones. Nature 257, 674675.
Toyama, K., Kimura, M. & Tanaka, K. (1981). Cross-correlation analysis of interneural connectivity in cat visual cortex. Journal of Neurophysiology 46, 191201.
Tsumoto, T., Eckart, W. & Creutzfeldt, O.D. (1979). Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition. Experimental Brain Research 34, 351363.
Vidyasagar, T.R. & Urbas, J.V. (1982). Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18. Experimental Brain Research 46, 157169.
Watson, A.B. (1987). Efficiency of human visual image codes. Investigative Ophthalmology and Visual Science (Suppl.) 28, 365.



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