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

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.

[1]  R. Shapley,et al.  Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. , 1991, Journal of neurophysiology.

[2]  R Linsker,et al.  From basic network principles to neural architecture: emergence of spatial-opponent cells. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[3]  D. Ferster Spatially opponent excitation and inhibition in simple cells of the cat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  J. Movshon,et al.  Spatial summation in the receptive fields of simple cells in the cat's striate cortex. , 1978, The Journal of physiology.

[5]  D. G. Albrecht,et al.  Spatial frequency selectivity of cells in macaque visual cortex , 1982, Vision Research.

[6]  A. Sillito The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the cat's striate cortex. , 1975, The Journal of physiology.

[7]  P. O. Bishop,et al.  Orientation specificity and response variability of cells in the striate cortex. , 1973, Vision research.

[8]  J. P. Jones,et al.  The two-dimensional spatial structure of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[9]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[10]  D. Hubel,et al.  Integrative action in the cat's lateral geniculate body , 1961, The Journal of physiology.

[11]  D. Hubel,et al.  Laminar and columnar distribution of geniculo‐cortical fibers in the macaque monkey , 1972, The Journal of comparative neurology.

[12]  P. Heggelund,et al.  Receptive field organization of simple cells in cat striate cortex , 1981, Experimental brain research.

[13]  B R Payne,et al.  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. , 1983, Journal of neurophysiology.

[14]  P. Somogyi,et al.  Evidence for interlaminar inhibitory circuits in the striate cortex of the cat , 1987, The Journal of comparative neurology.

[15]  D. Hubel,et al.  The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain , 1975, The Journal of comparative neurology.

[16]  S. Shapiro,et al.  An Analysis of Variance Test for Normality (Complete Samples) , 1965 .

[17]  P. Heggelund Quantitative studies of enhancement and suppression zones in the receptive field of simple cells in cat striate cortex. , 1986, The Journal of physiology.

[18]  I. Ohzawa,et al.  Contrast gain control in the cat's visual system. , 1985, Journal of neurophysiology.

[19]  A. B. Bonds Role of Inhibition in the Specification of Orientation Selectivity of Cells in the Cat Striate Cortex , 1989, Visual Neuroscience.

[20]  D. G. Albrecht,et al.  Motion selectivity and the contrast-response function of simple cells in the visual cortex , 1991, Visual Neuroscience.

[21]  J. P. Jones,et al.  An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[22]  D. Hubel,et al.  Effects of sleep and arousal on the processing of visual information in the cat , 1981, Nature.

[23]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[24]  S Marcelja,et al.  Mathematical description of the responses of simple cortical cells. , 1980, Journal of the Optical Society of America.

[25]  A. Sillito Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. , 1979, The Journal of physiology.

[26]  A M Aertsen,et al.  Reverse-correlation methods in auditory research , 1983, Quarterly Reviews of Biophysics.

[27]  R. A. Brooks,et al.  Principles of computer assisted tomography (CAT) in radiographic and radioisotopic imaging , 1976, Physics in medicine and biology.

[28]  L. Maffei,et al.  The visual cortex as a spatial frequency analyser. , 1973, Vision research.

[29]  S. Iversen,et al.  Handbook of Psychopharmacology , 1988, Springer US.

[30]  J. Movshon,et al.  The statistical reliability of signals in single neurons in cat and monkey visual cortex , 1983, Vision Research.

[31]  S. Blomfield Arithmetical operations performed by nerve cells. , 1974, Brain research.

[32]  T. Wiesel,et al.  The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat , 1990, Vision Research.

[33]  D. Burr,et al.  Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[34]  Albert Macovski,et al.  Medical imaging systems , 1983 .

[35]  P. O. Bishop,et al.  Receptive fields of simple cells in the cat striate cortex , 1973, The Journal of physiology.

[36]  D. Tolhurst,et al.  The effect of threshold on the relationship between the receptive-field profile and the spatial-frequency tuning cure in simple cells of the cat's striate cortex , 1989, Visual Neuroscience.

[37]  G. J. Tomko,et al.  Neuronal variability: non-stationary responses to identical visual stimuli. , 1974, Brain research.

[38]  D. G. Albrecht,et al.  Visual cortical neurons: are bars or gratings the optimal stimuli? , 1980, Science.

[39]  A. B. Bonds,et al.  Visual resolution and sensitivity of single cells in the primary visual cortex (V1) of a nocturnal primate (bush baby): correlations with cortical layers and cytochrome oxidase patterns. , 1993, Journal of neurophysiology.

[40]  J. Daugman Uncertainty relation for resolution in space, spatial frequency, and orientation optimized by two-dimensional visual cortical filters. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[41]  A. B. Bonds,et al.  Inhibitory refinement of spatial frequency selectivity in single cells of the cat striate cortex , 1991, Vision Research.

[42]  Donald A. Norman,et al.  Human Information Processing. , 1971 .

[43]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. , 1993, Journal of neurophysiology.

[44]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[45]  C. Gilbert,et al.  Generation of end-inhibition in the visual cortex via interlaminar connections , 1986, Nature.

[46]  P. O. Bishop,et al.  Responses to visual contours: spatio‐temporal aspects of excitation in the receptive fields of simple striate neurones , 1971, The Journal of physiology.

[47]  R. W. Rodieck,et al.  Analysis of receptive fields of cat retinal ganglion cells. , 1965, Journal of neurophysiology.

[48]  C. Gilbert Microcircuitry of the visual cortex. , 1983, Annual review of neuroscience.

[49]  K. Miller,et al.  Ocular dominance column development: analysis and simulation. , 1989, Science.

[50]  T. Wiesel,et al.  Clustered intrinsic connections in cat visual cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.