A Model of Neuronal Responses in Visual

Electrophysiological studies indicate that neurons in the middle temporal (MT) area of the primate brain are selective for the velocity of visual stimuli. This paper describes a computational model of MT physiology, in which local image velocities are represented via the distribution of MT neuronal responses. The computation is performed in two stages, corresponding to neurons in cortical areas V1 and MT. Each stage computes a weighted linear sum of inputs, followed by rectification and divisive normalization. V1 receptive field weights are designed for orientation and direction selectivity. MT receptive field weights are designed for velocity (both speed and direction) selectivity. The paper includes computational simulations accounting for a wide range of physiological data, and describes experiments that could be used to further test and refine the model. ©1998 Elsevier Science Ltd. All rights reserved.

[1]  S. Zeki,et al.  Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. , 1971, Brain research.

[2]  N. Logothetis,et al.  Neuronal correlates of subjective visual perception. , 1989, Science.

[3]  John H. R. Maunsell,et al.  Visual processing in monkey extrastriate cortex. , 1987, Annual review of neuroscience.

[4]  D J Heeger,et al.  Model for the extraction of image flow. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[5]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[6]  T. D. Albright,et al.  Transparency and coherence in human motion perception , 1990, Nature.

[7]  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.

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

[9]  P. McOwan,et al.  A computational model of the analysis of some first-order and second-order motion patterns by simple and complex cells , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  D. G. Albrecht,et al.  Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. , 1984, The Journal of physiology.

[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]  Edward H. Adelson,et al.  The Design and Use of Steerable Filters , 1991, IEEE Trans. Pattern Anal. Mach. Intell..

[13]  M. Carandini,et al.  Summation and division by neurons in primate visual cortex. , 1994, Science.

[14]  Claude L. Fennema,et al.  Velocity determination in scenes containing several moving objects , 1979 .

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

[16]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  E. Adelson,et al.  Phenomenal coherence of moving visual patterns , 1982, Nature.

[18]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[21]  W. Newsome,et al.  Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  E. Adelson,et al.  The analysis of moving visual patterns , 1985 .

[23]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[24]  I. Ohzawa,et al.  Organization of suppression in receptive fields of neurons in cat visual cortex. , 1992, Journal of neurophysiology.

[25]  Thomas D. Albright,et al.  Neural correlates of perceptual motion coherence , 1992, Nature.

[26]  John H. R. Maunsell,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. II. Binocular interactions and sensitivity to binocular disparity. , 1983, Journal of neurophysiology.

[27]  T. Sejnowski,et al.  A selection model for motion processing in area MT of primates , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  J. van Santen,et al.  Elaborated Reichardt detectors. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[29]  D. Heeger Modeling simple-cell direction selectivity with normalized, half-squared, linear operators. , 1993, Journal of neurophysiology.

[30]  G Sperling,et al.  Two motion perception mechanisms revealed through distance-driven reversal of apparent motion. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[31]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[32]  T D Albright,et al.  Form-cue invariant motion processing in primate visual cortex. , 1992, Science.

[33]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[34]  Andrew B. Watson,et al.  A look at motion in the frequency domain , 1983 .

[35]  G. Sperling,et al.  Drift-balanced random stimuli: a general basis for studying non-Fourier motion perception. , 1988, Journal of the Optical Society of America. A, Optics and image science.

[36]  H R Wilson,et al.  A model for motion coherence and transparency , 1994, Visual Neuroscience.

[37]  G. F. Cooper,et al.  The angular selectivity of visual cortical cells to moving gratings , 1968, The Journal of physiology.

[38]  Richard A. Young,et al.  Physiological model of motion analysis for machine vision , 1993, Electronic Imaging.

[39]  D. Burr,et al.  Seeing objects in motion , 1986, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[40]  A. T. Smith,et al.  Directional tuning interactions between moving oriented and textured stimuli in complex cells of feline striate cortex. , 1983, The Journal of physiology.

[41]  K. Tanaka,et al.  Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  Margaret E. Sereno Neural Computation of Pattern Motion: Modeling Stages of Motion Analysis in the Primate Visual Cortex , 1993 .

[43]  Keith Langley,et al.  Computational analysis of non-Fourier motion , 1994, Vision Research.

[44]  J. Movshon,et al.  Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex , 1997, The Journal of Neuroscience.

[45]  T D Albright,et al.  Cortical processing of visual motion. , 1993, Reviews of oculomotor research.

[46]  Eero P. Simoncelli,et al.  Computational models of cortical visual processing. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[48]  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.

[49]  Roger B. H. Tootell,et al.  Segregation of global and local motion processing in primate middle temporal visual area , 1992, Nature.

[50]  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.

[51]  J Allman,et al.  Direction- and Velocity-Specific Responses from beyond the Classical Receptive Field in the Middle Temporal Visual Area (MT) , 1985, Perception.

[52]  D. Heeger Nonlinear model of neural responses in cat visual cortex. , 1991 .

[53]  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.

[54]  T. Albright Direction and orientation selectivity of neurons in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[55]  K. H. Britten,et al.  Neuronal correlates of a perceptual decision , 1989, Nature.

[56]  P. Cavanagh,et al.  Motion: the long and short of it. , 1989, Spatial vision.

[57]  G. Orban,et al.  Speed and direction selectivity of macaque middle temporal neurons. , 1993, Journal of neurophysiology.

[58]  Edward H. Adelson,et al.  The extraction of Spatio-temporal Energy in Human and Machine Vision , 1997 .

[59]  W. Newsome,et al.  Directional pursuit deficits following lesions of the foveal representation within the superior temporal sulcus of the macaque monkey. , 1987, Journal of neurophysiology.

[60]  H. Rodman,et al.  Coding of visual stimulus velocity in area MT of the macaque , 1987, Vision Research.

[61]  G. F. Cooper,et al.  The spatial selectivity of the visual cells of the cat , 1969, The Journal of physiology.

[62]  John H. R. Maunsell,et al.  Topographic organization of the middle temporal visual area in the macaque monkey: Representational biases and the relationship to callosal connections and myeloarchitectonic boundaries , 1987, The Journal of comparative neurology.

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

[64]  Eero P. Simoncelli,et al.  Testing and refining a computational model of neural responses in area MT , 1996 .

[65]  R Shapley,et al.  Visual sensitivity and parallel retinocortical channels. , 1990, Annual review of psychology.

[66]  D. G. Albrecht,et al.  Visual cortical receptive fields in monkey and cat: Spatial and temporal phase transfer function , 1989, Vision Research.

[67]  W. Newsome,et al.  Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT. , 1986, Journal of neurophysiology.

[68]  J A Movshon,et al.  Visual cortical signals supporting smooth pursuit eye movements. , 1990, Cold Spring Harbor Symposia on Quantitative Biology.

[69]  D. Heeger,et al.  Contrast normalization and a linear model for the directional selectivity of simple cells in cat striate cortex , 1997, Visual Neuroscience.

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

[71]  D. Sparks,et al.  Size and distribution of movement fields in the monkey superior colliculus , 1976, Brain Research.

[72]  F. A. Miles,et al.  Visual Motion and Its Role in the Stabilization of Gaze , 1992 .

[73]  P. Hammond,et al.  Influence of velocity on directional tuning of complex cells in cat striate cortex for texture motion , 1980, Neuroscience Letters.

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

[75]  H. Wilson,et al.  A psychophysically motivated model for two-dimensional motion perception , 1992, Visual Neuroscience.

[76]  B. Knight,et al.  Contrast gain control in the primate retina: P cells are not X-like, some M cells are , 1992, Visual Neuroscience.

[77]  T. Poggio,et al.  Visual hyperacuity: spatiotemporal interpolation in human vision , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[78]  R. Andersen,et al.  Transparent motion perception as detection of unbalanced motion signals. II. Physiology , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  D. Heeger,et al.  Modeling the Apparent Frequency-specific Suppression in Simple Cell Responses , 1997, Vision Research.

[80]  Keith Langley,et al.  Recursive Filters for Optical Flow , 1995, IEEE Trans. Pattern Anal. Mach. Intell..

[81]  R. Andersen,et al.  Integration of motion and stereopsis in middle temporal cortical area of macaques , 1995, Nature.

[82]  W. Newsome,et al.  Microstimulation in visual area MT: effects on direction discrimination performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[83]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[84]  David J. Heeger,et al.  Model of visual motion sensing , 1994 .

[85]  D. Heeger,et al.  Comparison of contrast-normalization and threshold models of the responses of simple cells in cat striate cortex , 1997, Visual Neuroscience.

[86]  K. H. Britten,et al.  Responses of neurons in macaque MT to stochastic motion signals , 1993, Visual Neuroscience.

[87]  J. Movshon,et al.  Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex. , 1990, Journal of neurophysiology.

[88]  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.

[89]  Daniel A. Pollen,et al.  Visual cortical neurons as localized spatial frequency filters , 1983, IEEE Transactions on Systems, Man, and Cybernetics.

[90]  R A Andersen,et al.  The response of area MT and V1 neurons to transparent motion , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[91]  C. Enroth-Cugell,et al.  Chapter 9 Visual adaptation and retinal gain controls , 1984 .

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

[93]  Christof Koch,et al.  Computing Optical Flow in the Primate Visual System , 1989, Neural Computation.

[94]  A. Yuille,et al.  A model for the estimate of local image velocity by cells in the visual cortex , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[95]  Norberto M. Grzywacz,et al.  A Local Model for Transparent Motions Based on Spatio-Temporal Filters , 1993 .