Space-time maps and two-bar interactions of different classes of direction-selective cells in macaque V-1.

We used one-dimensional sparse noise stimuli to generate first-order spatiotemporal maps and second-order two-bar interaction maps for 65 simple and 124 complex direction-selective cells in alert macaque V1. Spatial and temporal phase differences between light and dark space-time maps clearly distinguished simple and complex cell populations. Complex cells usually showed similar direction preferences to light and dark bars, but many of the directional simple cells were much more direction selective to one sign of contrast than the reverse. We show that this is predicted by a simple energy model. Some of the direction-selective simple cells showed multiple space-time-slanted subregions, but others (previously described as S1 cells) had space-time maps that looked like just one subregion of an ordinary simple cell. Both simple and complex cells showed directional interactions (nonlinearities) to pairs of flashed bars (a 2-bar apparent-motion stimulus). The space-time slant of the simple cells correlated with the optimum dX/dT (velocity) of the paired-bar interactions. Some complex cells also showed a space-time slant; the direction of the slant usually correlated with the preferred direction of motion, but the degree of slant correlated with the inferred velocity tuning only when measured by a weighted-centroid calculation. Principal components analysis of the simple-cell space-time maps yielded one fast temporally biphasic component and a slower temporally monophasic component. We saw no consistent pattern for the spatial phase of the components, unlike previous reports; however, we show that principal components analysis may not distinguish between spatial offsets and phase offsets.

[1]  A. Sillito Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex , 1977, The Journal of physiology.

[2]  D. Ringach,et al.  On the classification of simple and complex cells , 2002, Vision Research.

[3]  D. Hubel Single unit activity in striate cortex of unrestrained cats , 1959, The Journal of physiology.

[4]  M. Tachibana,et al.  A Key Role of Starburst Amacrine Cells in Originating Retinal Directional Selectivity and Optokinetic Eye Movement , 2001, Neuron.

[5]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. I. Spatiotemporal organization of receptive fields. , 1976, Journal of neurophysiology.

[6]  Dendritic computation of direction selectivity by retinal ganglion cells. , 2000, Science.

[7]  D. Hubel,et al.  Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. , 1966, Journal of neurophysiology.

[8]  John H. R. Maunsell,et al.  Visual response latencies of magnocellular and parvocellular LGN neurons in macaque monkeys , 1999, Visual Neuroscience.

[9]  R. Marrocco,et al.  Sustained and transient cells in monkey lateral geniculate nucleus: conduction velocites and response properties. , 1976, Journal of neurophysiology.

[10]  T. Nealey,et al.  Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Anthony J. Movshon,et al.  Visual Response Properties of Striate Cortical Neurons Projecting to Area MT in Macaque Monkeys , 1996, The Journal of Neuroscience.

[12]  A J Ahumada,et al.  Model of human visual-motion sensing. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[13]  R. C. Emerson,et al.  Simple striate neurons in the cat. II. Mechanisms underlying directional asymmetry and directional selectivity. , 1977, Journal of neurophysiology.

[14]  R. L. de Valois,et al.  Inputs to directionally selective simple cells in macaque striate cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[15]  R. Reid,et al.  Synaptic Integration in Striate Cortical Simple Cells , 1998, The Journal of Neuroscience.

[16]  P. Schiller,et al.  Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. , 1978, Journal of neurophysiology.

[17]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[18]  D. Tolhurst,et al.  On the distinctness of simple and complex cells in the visual cortex of the cat. , 1983, The Journal of physiology.

[19]  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.

[20]  D H Hubel,et al.  Visual responses in V1 of freely viewing monkeys. , 1996, Cold Spring Harbor symposia on quantitative biology.

[21]  S. Deans The Radon Transform and Some of Its Applications , 1983 .

[22]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[23]  D. Tolhurst,et al.  Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex , 1991, Visual Neuroscience.

[24]  Doris Y. Tsao,et al.  Receptive fields of disparity-selective neurons in macaque striate cortex , 1999, Nature Neuroscience.

[25]  L. Palmer,et al.  Contribution of linear spatiotemporal receptive field structure to velocity selectivity of simple cells in area 17 of cat , 1989, Vision Research.

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

[27]  Curtis L. Baker,et al.  Space-time separability of direction selectivity in cat striate cortex neurons , 1988, Vision Research.

[28]  L. Palmer,et al.  Contribution of linear mechanisms to the specification of local motion by simple cells in areas 17 and 18 of the cat , 1994, Visual Neuroscience.

[29]  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.

[30]  O. D. Creutzfeldt,et al.  A quantitative study of chromatic organisation and receptive fields of cells in the lateral geniculate body of the rhesus monkey , 1979, Experimental Brain Research.

[31]  M. A. Repucci,et al.  Spatial Structure and Symmetry of Simple-Cell Receptive Fields in Macaque Primary Visual Cortex , 2002 .

[32]  A. L. Humphrey,et al.  Evidence of input from lagged cells in the lateral geniculate nucleus to simple cells in cortical area 17 of the cat. , 1992, Journal of neurophysiology.

[33]  N. Logothetis,et al.  Role of the color-opponent and broad-band channels in vision , 1990, Visual Neuroscience.

[34]  Klein,et al.  Nonlinear directionally selective subunits in complex cells of cat striate cortex. , 1987, Journal of neurophysiology.

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

[36]  Lawrence E. Marks,et al.  SPATIAL SUMMATION IN THE WARMTH SENSE , 1974 .

[37]  R. W. Rodieck,et al.  Identification, classification and anatomical segregation of cells with X‐like and Y‐like properties in the lateral geniculate nucleus of old‐world primates. , 1976, The Journal of physiology.

[38]  J. Movshon,et al.  Receptive field organization of complex cells in the cat's striate cortex. , 1978, The Journal of physiology.

[39]  C. Baker,et al.  Linear filtering and nonlinear interactions in direction-selective visual cortex neurons: A noise correlation analysis , 2001, Visual Neuroscience.

[40]  D N Mastronarde,et al.  Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells. , 1987, Journal of neurophysiology.

[41]  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.

[42]  Judson P. Jones,et al.  RECEPTIVE FIELD ORGANIZATION IN CAT AREA 17 , 1982 .

[43]  R. C. Emerson Quadrature subunits in directionally selective simple cells: Spatiotemporal interactions , 1997, Visual Neuroscience.

[44]  G. Henry,et al.  Direction selectivity of complex cells in a comparison with simple cells. , 1975, Journal of neurophysiology.

[45]  D. Heeger Half-squaring in responses of cat striate cells , 1992, Visual Neuroscience.

[46]  D. Hubel Tungsten Microelectrode for Recording from Single Units. , 1957, Science.

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

[48]  G. Henry Receptive field classes of cells in the striate cortex of the cat , 1977, Brain Research.

[49]  L. Palmer,et al.  Temporal diversity in the lateral geniculate nucleus of cat , 1998, Visual Neuroscience.

[50]  J. Hartigan,et al.  The Dip Test of Unimodality , 1985 .

[51]  Richard H. Masland,et al.  Retinal direction selectivity after targeted laser ablation of starburst amacrine cells , 1997, Nature.

[52]  Margaret S Livingstone,et al.  Two-Dimensional Substructure of MT Receptive Fields , 2001, Neuron.

[53]  M. Livingstone,et al.  Mechanisms of Direction Selectivity in Macaque V1 , 1998, Neuron.

[54]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[55]  M. C. Citron,et al.  White noise analysis of cortical directional selectivity in cat , 1983, Brain Research.

[56]  M. London,et al.  Dendritic computation. , 2005, Annual review of neuroscience.

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

[58]  D N Mastronarde,et al.  Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. , 1987, Journal of neurophysiology.

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

[60]  D. Pollen,et al.  Space-time spectra of complex cell filters in the macaque monkey: A comparison of results obtained with pseudowhite noise and grating stimuli , 1994, Visual Neuroscience.

[61]  J. H. Zar,et al.  Biostatistical Analysis (5th Edition) , 1984 .

[62]  T. Tsumoto,et al.  Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition , 1979, Experimental Brain Research.

[63]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

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

[65]  Bevil R. Conway,et al.  Spatial Structure of Cone Inputs to Color Cells in Alert Macaque Primary Visual Cortex (V-1) , 2001, The Journal of Neuroscience.

[66]  D. Ferster,et al.  Direction selectivity of synaptic potentials in simple cells of the cat visual cortex. , 1997, Journal of neurophysiology.

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

[68]  A. Sillito The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

[69]  A L Humphrey,et al.  Laminar differences in the spatiotemporal structure of simple cell receptive fields in cat area 17 , 1997, Visual Neuroscience.

[70]  I. Ohzawa,et al.  Encoding of binocular disparity by complex cells in the cat's visual cortex. , 1996, Journal of neurophysiology.

[71]  Russell L. De Valois,et al.  PII: S0042-6989(00)00210-8 , 2000 .

[72]  E. Adelson,et al.  Directionally selective complex cells and the computation of motion energy in cat visual cortex , 1992, Vision Research.

[73]  A. L. Humphrey,et al.  Inhibitory contributions to spatiotemporal receptive-field structure and direction selectivity in simple cells of cat area 17. , 1999, Journal of neurophysiology.