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Two-dimensional receptive-field organization in striate cortical neurons of the cat

Published online by Cambridge University Press:  02 June 2009

Ming Sun
Affiliation:
Departments of Biomedical and Electrical Engineering, Vanderbilt University, Nashville
A. B. Bonds
Affiliation:
Departments of Biomedical and Electrical Engineering, Vanderbilt University, Nashville

Abstract

The two-dimensional organization of receptive fields (RFs) of 44 cells in the cat visual cortex and four cells from the cat LGN was measured by stimulation with either dots or bars of light. The light bars were presented in different positions and orientations centered on the RFs. The RFs found were arbitrarily divided into four general types: Punctate, resembling DOG filters (11%); those resembling Gabor filters (9%); elongate (36%); and multipeaked-type (44%). Elongate RFs, usually found in simple cells, could show more than one excitatory band or bifurcation of excitatory regions. Although regions inhibitory to a given stimulus transition (e.g. ON) often coincided with regions excitatory to the opposite transition (e.g. OFF), this was by no means the rule. Measurements were highly repeatable and stable over periods of at least 1 h. A comparison between measurements made with dots and with bars showed reasonable matches in about 40% of the cases. In general, bar-based measurements revealed larger RFs with more structure, especially with respect to inhibitory regions. Inactivation of lower cortical layers (V-VI) by local GABA injection was found to reduce sharpness of detail and to increase both receptive-field size and noise in upper layer cells, suggesting vertically organized RF mechanisms. Across the population, some cells bore close resemblance to theoretically proposed filters, while others had a complexity that was clearly not generalizable, to the extent that they seemed more suited to detection of specific structures. We would speculate that the broadly varying forms of cat cortical receptive fields result from developmental processes akin to those that form ocular-dominance columns, but on a smaller scale.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

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References

Albrecht, D.G., DeValois, R.L. & Thorell, L.G. (1980). Visual cortical neurons: Are bars or gratings the optimal stimuli? Science 207, 8890.CrossRefGoogle ScholarPubMed
Albrecht, D.G. & Geisler, W.S. (1991). Motion selectivity and the contrast-response function of simple cells in the visual cortex. Visual Neuroscience, 7, 531546.CrossRefGoogle ScholarPubMed
Bauman, L.A. & Bonds, A.B. (1991). Inhibitory refinement of spatial frequency selectivity in single cells of the cat striate cortex. Vision Research 31, 933944.CrossRefGoogle ScholarPubMed
Bishop, P.O., Coombs, J.S. & Henry, G.H. (1971). Responses to visual contours: Spatio-temporal aspects of excitation in the receptive fields of simple striate neurons. Journal of Physiology 219, 625657.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Blomfield, S. (1974). Arithmetical operations performed by nerve cells. Brain Research 69, 115124.CrossRefGoogle ScholarPubMed
Bolz, J. & Gilbert, C.D. (1986). Generation of end-inhibition in the visual cortex via interlaminar connections. Nature 320, 362.CrossRefGoogle ScholarPubMed
Bonds, A.B. (1989). Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Visual Neuroscience 2, 4155.CrossRefGoogle ScholarPubMed
Bonds, A.B. (1992). Spatial and temporal non-linearities in the receptive fields of striate cortical cells. In Non-Linear Vision, ed. Pinter, R.B. & Nabet, B., pp. 329352. Boca Raton, Florida: CRC Press Cybernetics Series.Google Scholar
Brooks, R.A. & Giovanni, D.C. (1976). Principles of computer assisted tomography (CAT) in radiographic and radioisotopic imaging. Physiological Medicine and Biology 21, 689732.CrossRefGoogle ScholarPubMed
Daugman, J.G. (1985). Uncertainty relation for resolution in space, spatial frequency and orientation optimized by two-dimensional cortical filters. Journal of the Optical Society of America A 2, 11601169.CrossRefGoogle ScholarPubMed
DeAngelis, G.C., Ohzawa, I. & Freeman, R.D. (1993). Spatiotem poral organization of simple-cell receptive fields in cat's striate cortex. II. Linearity of temporal and spatial summation. Journal of Neurophysiology 69, 11181135.CrossRefGoogle Scholar
DeBruyn, E.J., Casagrande, V.A., Beck, P. & Bonds, A.B. (1993). Characteristics of single units in striate cortex of a nocturnal prosimian, Galago Crassicaudatus. Journal of Neurophysiology 69, 318.CrossRefGoogle Scholar
DeValois, R.L., Albrecht, D.G. & Thorell, L.G. (1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545559.CrossRefGoogle Scholar
Eggermont, J.J., Johannesma, P.I.M. & Aertsen, A.M.H.J. (1983). Reverse-correlation methods in auditory research. Quarterly Review of Biophysics 16, 341414.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517552.CrossRefGoogle ScholarPubMed
Ferster, D. (1988). Spatially opponent excitation and inhibition in simple cells of the cat visual cortex. Journal of Neuroscience 8, 11721180.CrossRefGoogle ScholarPubMed
Gilbert, C.D. (1983). Microcircuitry of cat visual cortex. Annual Review of Neuroscience 6, 217247.CrossRefGoogle Scholar
Gilbert, C.D. & Wiesel, T.N. (1983). Clustered intrinsic connections in the cat visual cortex. Journal of Neuroscience 3, 11161133.CrossRefGoogle ScholarPubMed
Gilbert, C.D. & Wiesel, T.N. (1990). The influence of contextual stimuli on the orientation selectivity of cells in the primary visual cortex of the cat. Vision Research 30, 16891701.CrossRefGoogle ScholarPubMed
Heggelund, P. (1981 a). Receptive field organization of simple cells in cat striate cortex. Experimental Brain Research 42, 8998.Google ScholarPubMed
Heggelund, P. (1981 b). Receptive field organization of complex cells in cat striate cortex. Experimental Brain Research 42, 99107.Google ScholarPubMed
Heggelund, P. (1986). Quantitative studies of enhancement and suppression zones in the receptive field of simple cells in cat striate cortex. Journal of Physiology 373, 293310.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1961). Integrative action in the cat's lateral geniculate body. Journal of Physiology 155, 385398.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Hubel, D.H. & WIesel, T.N. (1972). Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421450.CrossRefGoogle ScholarPubMed
Jones, J.P. & Palmer, L.A. (1987 a). The two-dimensional spatial structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 11871211.CrossRefGoogle ScholarPubMed
Jones, J.P. & Palmer, L.A. (1987 b). An evaluation of the two dimensional Gabor filter model of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 12331258.CrossRefGoogle ScholarPubMed
Kelly, J.S. (1975). Microiontophoretic application of drugs onto single neurons. In Handbook of Psychopharmacology Vol. 2, ed. Iverson, L.L., Iverson, S.D., & Snyder, S.H., pp. 2967. New York: Plenum Press.Google Scholar
Kisvarday, Z.F., Martin, K.A.C., Friedlander, M.J. & Somogyi, P. (1987). Evidence for interlaminar inhibitory circuits in the striate cortex of the cat. Journal of Comparative Neurology 260, 119.CrossRefGoogle ScholarPubMed
LeVay, S., Hubel, D.H. & Wiesel, T.N. (1975). The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain. Journal of Comparative Neurology 159, 559576.CrossRefGoogle ScholarPubMed
Lindsay, P.M. & Norman, D.A. (1972). Human Information Processing. New York: Academic Press.Google Scholar
Linsker, R. (1986). From basic network principles to neural architecture: Emergence of spatial-opponent cells. Proceedings of the National Academy of Sciences of the U.S.A. 83, 75087512.Google Scholar
Livingstone, M.S. & Hubel, D.H. (1981). Effects of sleep and arousal on the processing of visual information in the cat. Nature 291, 554561.CrossRefGoogle ScholarPubMed
Macovski, A. (1980). Medical Imaging Systems, ed. Schmitt, R.O. et al. , pp. 105124. Englewood Cliffs, NJ: Prentice-Hall Inc.Google Scholar
Maffei, L. & Fiorentini, A. (1973). The visual cortex as a spatial frequency analyser. Vision Research 13, 12551267.Google Scholar
Marcelja, S. (1980). Mathematical description of the responses of simple cortical cells. Journal of the Optical Society of America 70, 12971300.CrossRefGoogle ScholarPubMed
Miller, K.D., Keller, J.B. & Stryker, M.P. (1989). Ocular dominance column development: Analysis and simulation. Science 245, 605615.CrossRefGoogle ScholarPubMed
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 (London) 216, 335354.Google ScholarPubMed
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978). Spatial summation in the receptive fields of simple cells in the cat's striate cortex. Journal of Physiology 283, 5377.CrossRefGoogle ScholarPubMed
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat's visual system. Journal of Neurophysiology 54, 651667.CrossRefGoogle ScholarPubMed
Payne, B.R. & Berman, N. (1983). Functional organization of neurons in cat striate cortex: Variations in preferred orientation and orientation selectivity with receptive field type, ocular dominance and location in visual field map. Journal of Neurophysiology 49, 10511072.CrossRefGoogle ScholarPubMed
Reid, R.C., Soodak, R.E. & Shapley, R.M. (1991). Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. Journal of Neurophysiology 66, 505529.Google Scholar
Rodieck, R.S. & Stone, J.S. (1965). Analysis of receptive fields of cat retina ganglion cells. Journal of Neurophysiology 28, 965980.CrossRefGoogle Scholar
Rose, D. & Blakemore, C.B. (1974). An analysis of orientation selectivity in the cat's visual cortex. Experimental Brain Research 20, 117.CrossRefGoogle ScholarPubMed
Shapiro, S.S. & Wilk, M.B. (1965). Analysis of variance test for normality. Biometrika 52, 591611.CrossRefGoogle Scholar
Sillito, A.M. (1975). The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the cat's striate cortex. Journal of Physiology 250, 287304.CrossRefGoogle ScholarPubMed
Sillito, A.M. (1979). Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. Journal of Physiology 289, 3353.CrossRefGoogle ScholarPubMed
Tadmor, Y. & Tolhurst, D.J. (1989). The effect of threshold on the relationship between the receptive-field profile and the spatial-frequency tuning curve in simple cells of the cat's striate cortex. Visual Neuroscience 3, 445454.CrossRefGoogle ScholarPubMed
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, 755785.CrossRefGoogle Scholar
Tomko, G.J. & Crapper, D.R. (1974). Neuronal variability: Non-stationary responses to identical visual stimuli. Brain Research 79, 405418.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. Journal of Comparative Neurology 177, 213236.CrossRefGoogle ScholarPubMed
Valverde, F. (1985). The organizing principles of the primary visual cortex in the monkey. In Cerebral Cortex, Vol. 3, ed. Peters, A. & Jones, E.G., pp. 207257. New York: Plenum Press.Google Scholar