Receptive field dynamics underlying MST neuronal optic flow selectivity.

Optic flow informs moving observers about their heading direction. Neurons in monkey medial superior temporal (MST) cortex show heading selective responses to optic flow and planar direction selective responses to patches of local motion. We recorded MST neuronal responses to a 90 x 90 degrees optic flow display and to a 3 x 3 array of local motion patches covering the same area. Our goal was to test the hypothesis that the optic flow responses reflect the sum of the local motion responses. The local motion responses of each neuron were modeled as mixtures of Gaussians, combining the effects of two Gaussian response functions derived using a genetic algorithm, and then used to predict that neuron's optic flow responses. Some neurons showed good correspondence between local motion models and optic flow responses, others showed substantial differences. We used the genetic algorithm to modulate the relative strength of each local motion segment's responses to accommodate interactions between segments that might modulate their relative efficacy during co-activation by global patterns of optic flow. These gain modulated models showed uniformly better fits to the optic flow responses, suggesting that coactivation of receptive field segments alters neuronal response properties. We tested this hypothesis by simultaneously presenting local motion stimuli at two different sites. These two-segment stimuli revealed that interactions between response segments have direction and location specific effects that can account for aspects of optic flow selectivity. We conclude that MST's optic flow selectivity reflects dynamic interactions between spatially distributed local planar motion response mechanisms.

[1]  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.

[2]  S. Zeki The response properties of cells in the middle temporal area (area MT) of owl monkey visual cortex , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[3]  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.

[4]  Ruye Wang A Simple Competitive Account of Some Response Properties of Visual Neurons in Area MSTd , 1995, Neural Computation.

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

[6]  R. Wurtz,et al.  Medial Superior Temporal Area Neurons Respond to Speed Patterns in Optic Flow , 1997, The Journal of Neuroscience.

[7]  Leslie G. Ungerleider,et al.  Subcortical connections of visual areas MST and FST in macaques , 1992, Visual Neuroscience.

[8]  Robert H. Wurtz,et al.  Multiple temporal components of optic flow responses in MST neurons , 1997, Experimental Brain Research.

[9]  Markus Lappe,et al.  A Neural Network for the Processing of Optic Flow from Ego-Motion in Man and Higher Mammals , 1993, Neural Computation.

[10]  T. Poggio,et al.  A parallel algorithm for real-time computation of optical flow , 1989, Nature.

[11]  Eero P. Simoncelli,et al.  A Model of Neuronal Responses in Visual , 1998 .

[12]  J. Lishman,et al.  The Autonomy of Visual Kinaesthesis , 1973, Perception.

[13]  Andrea J. van Doorn,et al.  Invariant Properties of the Motion Parallax Field due to the Movement of Rigid Bodies Relative to an Observer , 1975 .

[14]  A. V. van den Berg,et al.  Heading detection using motion templates and eye velocity gain fields , 1998, Vision Research.

[15]  K. Hoffmann,et al.  Optic Flow Processing in Monkey STS: A Theoretical and Experimental Approach , 1996, The Journal of Neuroscience.

[16]  J. Movshon,et al.  Adaptation changes the direction tuning of macaque MT neurons , 2004, Nature Neuroscience.

[17]  D. J. Felleman,et al.  Receptive-field properties of neurons in middle temporal visual area (MT) of owl monkeys. , 1984, Journal of neurophysiology.

[18]  W. Senn,et al.  Top-down dendritic input increases the gain of layer 5 pyramidal neurons. , 2004, Cerebral cortex.

[19]  Brian P. Dyre,et al.  Image velocity magnitudes and perception of heading. , 1997 .

[20]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[21]  Dora E Angelaki,et al.  Visual and Nonvisual Contributions to Three-Dimensional Heading Selectivity in the Medial Superior Temporal Area , 2006, The Journal of Neuroscience.

[22]  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.

[23]  Norberto M. Grzywacz,et al.  Parametric decomposition of optic flow by humans , 2005, Vision Research.

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

[25]  J. Perrone,et al.  A model of self-motion estimation within primate extrastriate visual cortex , 1994, Vision Research.

[26]  E. Batschelet Circular statistics in biology , 1981 .

[27]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. III. Interaction with full-field visual stimulation. , 1988, Journal of neurophysiology.

[28]  Eero P. Simoncelli,et al.  A model of neuronal responses in visual area MT , 1998, Vision Research.

[29]  Constance S. Royden,et al.  Differential effects of shared attention on perception of heading and 3-D object motion , 1999, Perception & psychophysics.

[30]  Erik De Schutter,et al.  Automated neuron model optimization techniques: a review , 2008, Biological Cybernetics.

[31]  Keiji Tanaka,et al.  Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[33]  Bartlett W. Mel,et al.  Dendrites: bug or feature? , 2003, Current Opinion in Neurobiology.

[34]  M. Graziano,et al.  Tuning of MST neurons to spiral motions , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  B. Sakmann,et al.  Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons , 2001, The Journal of physiology.

[36]  G. Orban,et al.  Spatial heterogeneity of inhibitory surrounds in the middle temporal visual area. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[37]  C. Duffy,et al.  Heading representation in MST: sensory interactions and population encoding. , 2003, Journal of neurophysiology.

[38]  Mamoru Nakanishi,et al.  A parallel algorithm for real-time object recognition , 2002, Pattern Recognit..

[39]  Xin Huang,et al.  Stimulus Dependency and Mechanisms of Surround Modulation in Cortical Area MT , 2008, The Journal of Neuroscience.

[40]  K. Tanaka,et al.  Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[41]  Markus Lappe,et al.  Local statistics of retinal optic flow for self-motion through natural sceneries , 2007, Network.

[42]  Markus Lappe,et al.  Circular receptive field structures for flow analysis and heading detection , 2004 .

[43]  W K Page,et al.  MST neuronal responses to heading direction during pursuit eye movements. , 1999, Journal of neurophysiology.

[44]  J. Movshon,et al.  Adaptive Temporal Integration of Motion in Direction-Selective Neurons in Macaque Visual Cortex , 2004, The Journal of Neuroscience.

[45]  葉維彰,et al.  The Grid System , 1939, Nature.

[46]  Leslie G. Ungerleider,et al.  Pathways for motion analysis: Cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque , 1990, The Journal of comparative neurology.

[47]  H. Rodman,et al.  Single-unit analysis of pattern-motion selective properties in the middle temporal visual area (MT) , 2004, Experimental Brain Research.

[48]  田中 啓治 Analysis of Local and Wide-Field Movements in the Superior Temporal Visual Areas of the Macaque Monkey , 1987 .

[49]  Frank Bremmer,et al.  Interaction of linear vestibular and visual stimulation in the macaque ventral intraparietal area (VIP) , 2002, The European journal of neuroscience.

[50]  K. Prazdny Determining The Instantaneous Direction Of Motion From Optical Flow Generated By A Curvilinearly Moving Observer , 1981, Other Conferences.

[51]  R. Wurtz,et al.  Response of monkey MST neurons to optic flow stimuli with shifted centers of motion , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  Markus Lappe,et al.  Efficient encoding of natural optic flow , 2008, Network.

[53]  L. Stone,et al.  The Barberplaid Illusion: Plaid Motion is Biased by Elongated Apertures , 1996, Vision Research.

[54]  Brian P. Dyre,et al.  Image velocity magnitudes and perception of heading. , 1997, Journal of experimental psychology. Human perception and performance.

[55]  R. D. Patterson,et al.  Using genetic algorithms to find the most effective stimulus for sensory neurons , 2003, Journal of Neuroscience Methods.

[56]  K. Hoffmann,et al.  Responses to continuously changing optic flow in area MST. , 2000, Journal of neurophysiology.

[57]  C. Duffy,et al.  Behavioral influences on cortical neuronal responses to optic flow. , 2007, Cerebral cortex.

[58]  K. H. Britten,et al.  Spatial Summation in the Receptive Fields of MT Neurons , 1999, The Journal of Neuroscience.

[59]  John H. R. Maunsell,et al.  Attentional modulation of visual motion processing in cortical areas MT and MST , 1996, Nature.

[60]  H. C. Longuet-Higgins,et al.  The interpretation of a moving retinal image , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[61]  C. Duffy,et al.  Optic flow illusion and single neuron behaviour reconciled by a population model , 1999, The European journal of neuroscience.

[62]  Lance M. Optican,et al.  Unix-based multiple-process system, for real-time data acquisition and control , 1982 .

[63]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[64]  Jack M. H. Beusmans,et al.  Computing the direction of heading from affine image flow , 1993, Biological Cybernetics.

[65]  Hidehiko Komatsu,et al.  A grid system and a microsyringe for single cell recording , 1988, Journal of Neuroscience Methods.

[66]  Kechen Zhang,et al.  Emergence of Position-Independent Detectors of Sense of Rotation and Dilation with Hebbian Learning: An Analysis , 1999, Neural Computation.

[67]  Hilary W. Heuer,et al.  Parietal Area VIP Neuronal Responses to Heading Stimuli Are Encoded in Head-Centered Coordinates , 2004, Neuron.

[68]  R. Desimone,et al.  Columnar organization of directionally selective cells in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[69]  J Duysens,et al.  Neurons in the ventral intraparietal area of awake macaque monkey closely resemble neurons in the dorsal part of the medial superior temporal area in their responses to optic flow patterns. , 1996, Journal of neurophysiology.

[70]  Leslie Welch,et al.  The perception of moving plaids reveals two motion-processing stages , 1989, Nature.

[71]  Leslie G. Ungerleider,et al.  Cortical connections of visual area MT in the macaque , 1986, The Journal of comparative neurology.

[72]  J. Anthony Movshon,et al.  Visual response properties of striate cortical neurons projecting to V2 in macaque , 2010 .

[73]  F. Bremmer,et al.  The use of optical velocities for distance discrimination and reproduction during visually simulated self motion , 1999, Experimental Brain Research.

[74]  Markus Lappe,et al.  Visual selectivity for heading in monkey area MST , 2009, Experimental Brain Research.

[75]  Christof Koch,et al.  Shunting Inhibition Does Not Have a Divisive Effect on Firing Rates , 1997, Neural Computation.

[76]  K. Mardia Statistics of Directional Data , 1972 .

[77]  James A. Crowell,et al.  The perception of heading during eye movements , 1992, Nature.

[78]  R. Wurtz,et al.  An illusory transformation of optic flow fields , 1993, Vision Research.

[79]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. , 1991, Journal of neurophysiology.

[80]  J. Maunsell,et al.  Effects of Attention on the Processing of Motion in Macaque Middle Temporal and Medial Superior Temporal Visual Cortical Areas , 1999, The Journal of Neuroscience.

[81]  J. Koenderink,et al.  Exterospecific component of the motion parallax field. , 1981, Journal of the Optical Society of America.

[82]  C. Duffy MST neurons respond to optic flow and translational movement. , 1998, Journal of neurophysiology.

[83]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[84]  Idan Segev,et al.  The Endurance and Selectivity of Spatial Patterns of Long-Term Potentiation/Depression in Dendrites under Homeostatic Synaptic Plasticity , 2006, The Journal of Neuroscience.

[85]  David J Logan,et al.  Cerebral Cortex doi:10.1093/cercor/bhj082 Cerebral Cortex Advance Access published December 7, 2005 Cortical Area MSTd Combines Visual Cues , 2022 .

[86]  Frank Bremmer,et al.  The Representation of Movement in Near Extra-Personal Space in the Macaque Ventral Intraparietal Area (VIP) , 1997 .

[87]  R. Andersen,et al.  Mechanisms of Heading Perception in Primate Visual Cortex , 1996, Science.

[88]  Kunihiko Fukushima,et al.  Neural network model for extracting optic flow , 2005, Neural Networks.

[89]  R. Wurtz,et al.  Planar directional contributions to optic flow responses in MST neurons. , 1997, Journal of neurophysiology.

[90]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: anatomic location and visual response properties. , 1993, Journal of neurophysiology.

[91]  Y. Diao,et al.  Sensitivity of LS neurons to optic flow stimuli , 1997 .

[92]  Markus Lappe,et al.  An illusory transformation in a model of optic flow processing , 1995, Vision Research.

[93]  K. Tanaka,et al.  Underlying mechanisms of the response specificity of expansion/contraction and rotation cells in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[94]  Brent Doiron,et al.  Subtractive and Divisive Inhibition: Effect of Voltage-Dependent Inhibitory Conductances and Noise , 2001, Neural Computation.

[95]  Alexandre Pouget,et al.  Probabilistic Interpretation of Population Codes , 1996, Neural Computation.

[96]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small-field stimuli. , 1991, Journal of neurophysiology.

[97]  J A Perrone,et al.  Model for the computation of self-motion in biological systems. , 1992, Journal of the Optical Society of America. A, Optics and image science.

[98]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. , 1988, Journal of neurophysiology.

[99]  James A. Crowell,et al.  Estimating heading during real and simulated eye movements , 1996, Vision Research.

[100]  Charles J. Duffy,et al.  Cortical Neurons Encoding Path and Place: Where You Go Is Where You Are , 2002, Science.

[101]  Eero P. Simoncelli,et al.  How MT cells analyze the motion of visual patterns , 2006, Nature Neuroscience.

[102]  D J Hannon,et al.  Eye movements and optical flow. , 1990, Journal of the Optical Society of America. A, Optics and image science.