Length and width tuning of neurons in the cat's primary visual cortex.

1. The classically defined receptive field of a visual neuron is the area of visual space over which the cell responds to visual stimuli. It is well established, however, that the discharge produced by an optimal stimulus can be modulated by the presence of additional stimuli that by themselves do not produce any response. This study examines inhibitory influences that originate from areas located outside of the classical (i.e., excitatory) receptive field. Previous work has shown that for some cells the response to a properly oriented bar of light becomes attenuated when the bar extends beyond the receptive field, a phenomenon known as end-inhibition (or length tuning). Analogously, it has been shown that increasing the number of cycles of a drifting grating stimulus may also inhibit the firing of some cells, an effect known as side-inhibition (or width tuning). Very little information is available, however, about the relationship between end- and side-inhibition. We have examined the spatial organization and tuning characteristics of these inhibitory effects by recording extracellularly from single neurons in the cat's striate cortex (Area 17). 2. For each cortical neuron, length and width tuning curves were obtained with the use of rectangular patches of drifting sinusoidal gratings that have variable length and width. Results from 82 cells show that the strengths of end- and side-inhibition tend to be correlated. Most cells that exhibit clear end-inhibition also show a similar degree of side-inhibition. For these cells, the excitatory receptive field is surrounded on all sides by inhibitory zones. Some cells exhibit only end- or side-inhibition, but not both. Data for 28 binocular cells show that length and width tuning curves for the dominant and nondominant eyes tend to be closely matched. 3. We also measured tuning characteristics of end- and side-inhibition. To obtain these data, the excitatory receptive field was stimulated with a grating patch having optimal orientation, spatial frequency, and size, whereas the end- or side-inhibitory regions were stimulated with patches of gratings that had a variable parameter (such as orientation). Results show that end- and side-inhibition tend to be strongest at the orientation and spatial frequency that yield maximal excitation. However, orientation and spatial frequency tuning curves for inhibition are considerably broader than those for excitation, suggesting that inhibition is mediated by a pool of neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  S. W. Kuffler Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[2]  W. Burke,et al.  Activation of Single Lateral eniculate Cells by Stimulation of Either Optic Nerve , 1959, Science.

[3]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[4]  S. Erulkar,et al.  Single‐unit activity in the lateral geniculate body of the cat , 1960, The Journal of physiology.

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

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

[7]  B JULESZ,et al.  Binocular Depth Perception without Familiarity Cues , 1964, Science.

[8]  D H HUBEL,et al.  RECEPTIVE FIELDS AND FUNCTIONAL ARCHITECTURE IN TWO NONSTRIATE VISUAL AREAS (18 AND 19) OF THE CAT. , 1965, Journal of neurophysiology.

[9]  O. Creutzfeldt,et al.  Significance of intracortical inhibition in the visual cortex. , 1972, Nature: New biology.

[10]  B. Dreher Hypercomplex cells in the cat's striate cortex. , 1972, Investigative ophthalmology.

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

[12]  K. Nakayama,et al.  A Velocity Analogue of Brightness Contrast , 1973, Perception.

[13]  K. Nakayama,et al.  Optical Velocity Patterns, Velocity-Sensitive Neurons, and Space Perception: A Hypothesis , 1974, Perception.

[14]  L Maffei,et al.  Behavioural contrast sensitivity of the cat in various visual meridians , 1974, The Journal of physiology.

[15]  R Blake,et al.  Visual resolution in the cat. , 1974, Vision research.

[16]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. III. Spatial frequency. , 1976, Journal of neurophysiology.

[17]  L. Maffei,et al.  The unresponsive regions of visual cortical receptive fields , 1976, Vision Research.

[18]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. , 1976, Journal of neurophysiology.

[19]  D. Pollen,et al.  Responses of complex cells in the visual cortex of the cat as a function of the length of moving slits , 1976, Brain Research.

[20]  A. Sillito,et al.  The contribution of excitatory and inhibitory inputs to the length preference of hypercomplex cells in layers II and III of the cat's striate cortex , 1977, The Journal of physiology.

[21]  K. Albus,et al.  Effects of interacting visual patterns on single cell responses in cat's striate cortex , 1977, Vision Research.

[22]  C. Gilbert Laminar differences in receptive field properties of cells in cat primary visual cortex , 1977, The Journal of physiology.

[23]  D. Rose Responses of single units in cat visual cortex to moving bars of light as a function of bar length , 1977, The Journal of physiology.

[24]  A. Sillito The spatial extent of excitatory and inhibitory zones in the receptive field of superficial layer hypercomplex cells , 1977, The Journal of physiology.

[25]  J. Nelson,et al.  Orientation-selective inhibition from beyond the classic visual receptive field , 1978, Brain Research.

[26]  P. O. Bishop,et al.  Hypercomplex and simple/complex cell classifications in cat striate cortex. , 1978, Journal of neurophysiology.

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

[28]  D. Rose Mechanisms underlying the receptive field properties of neurons in cat visual cortex , 1979, Vision Research.

[29]  P. O. Bishop,et al.  Dimensions and properties of end-zone inhibitory areas in receptive fields of hypercomplex cells in cat striate cortex. , 1979, Journal of neurophysiology.

[30]  P. O. Bishop,et al.  End-zone region in receptive fields of hypercomplex and other striate neurons in the cat. , 1979, Journal of neurophysiology.

[31]  A. P. Petrov,et al.  Some evidence against Fourier analysis as a function of the receptive fields in cat's striate cortex , 1980, Vision Research.

[32]  William H. Merigan,et al.  The luminance dependence of spatial vision in the cat , 1981, Vision Research.

[33]  P. O. Bishop,et al.  Binocular interaction on monocularly discharged lateral geniculate and striate neurons in the cat. , 1981, Journal of neurophysiology.

[34]  B. Julesz Textons, the elements of texture perception, and their interactions , 1981, Nature.

[35]  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.

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

[37]  K. D. De Valois,et al.  Spatial‐frequency‐specific inhibition in cat striate cortex cells. , 1983, The Journal of physiology.

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

[39]  K. Nakayama,et al.  Single visual neurons code opposing motion independent of direction. , 1983, Science.

[40]  D. G. Albrecht,et al.  Periodicity of striate-cortex-cell receptive fields. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[41]  H. Nothdurft,et al.  Texture discrimination: Representation of orientation and luminance differences in cells of the cat striate cortex , 1985, Vision Research.

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

[43]  P. O. Bishop,et al.  End-stopped cells and binocular depth discrimination in the striate cortex of cats , 1986, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[44]  I. Ohzawa,et al.  The binocular organization of simple cells in the cat's visual cortex. , 1986, Journal of neurophysiology.

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

[46]  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.

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

[48]  S. Zucker,et al.  Endstopped neurons in the visual cortex as a substrate for calculating curvature , 1987, Nature.

[49]  P. C. Murphy,et al.  Corticofugal feedback influences the generation of length tuning in the visual pathway , 1987, Nature.

[50]  C. Koch,et al.  Neuronal connections underlying orientation selectivity in cat visual cortex , 1987, Trends in Neurosciences.

[51]  G. Orban,et al.  Influence of a moving textured background on direction selectivity of cat striate neurons. , 1987, Journal of neurophysiology.

[52]  K. Martin,et al.  The Wellcome Prize lecture. From single cells to simple circuits in the cerebral cortex. , 1988, Quarterly journal of experimental physiology.

[53]  R. von der Heydt,et al.  Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[55]  R. von der Heydt,et al.  Mechanisms of contour perception in monkey visual cortex. II. Contours bridging gaps , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  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.

[57]  T. Wiesel,et al.  Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  B. Rogers,et al.  Disparity curvature and the perception of three-dimensional surfaces , 1989, Nature.

[59]  Ina Ruck,et al.  USA , 1969, The Lancet.

[60]  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.

[61]  I. Ohzawa,et al.  Stereoscopic depth discrimination in the visual cortex: neurons ideally suited as disparity detectors. , 1990, Science.

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

[63]  A. B. Bonds,et al.  Classifying simple and complex cells on the basis of response modulation , 1991, Vision Research.

[64]  R. Born,et al.  Single-unit and 2-deoxyglucose studies of side inhibition in macaque striate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[65]  H. Jones,et al.  The length‐response properties of cells in the feline dorsal lateral geniculate nucleus. , 1991, The Journal of physiology.

[66]  A. B. Bonds Temporal dynamics of contrast gain in single cells of the cat striate cortex , 1991, Visual Neuroscience.

[67]  T. Wiesel,et al.  Targets of horizontal connections in macaque primary visual cortex , 1991, The Journal of comparative neurology.

[68]  D. V. van Essen,et al.  Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. , 1992, Journal of neurophysiology.

[69]  R. von der Heydt,et al.  Periodic-pattern-selective cells in monkey visual cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  Olaf Kübler,et al.  Simulation of neural contour mechanisms: from simple to end-stopped cells , 1992, Vision Research.

[71]  Michael P. Stryker,et al.  Origin of orientation tuning in the visual cortex , 1992, Current Opinion in Neurobiology.

[72]  R. Freeman,et al.  Oscillatory discharge in the visual system: does it have a functional role? , 1992, Journal of neurophysiology.

[73]  D. Heeger Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

[74]  R D Freeman,et al.  Development of binocular vision in the kitten's striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[75]  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.

[76]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. , 1993, Journal of neurophysiology.