A model of encoding and decoding in V1 and MT accounts for motion perception anisotropies in the human visual system

We used the motion aftereffect (MAE) to psychophysically characterize tuning of motion perception in the human visual system. The function relating MAE strength and the range of directions present in the adapter stimulus provides information regarding the width of direction tuning of motion adaptation. We compared the directional anisotropy in MAE tuning width to the well-known oblique effect in motion direction discrimination. In agreement with previous research, we found that subjects had lower motion direction discrimination thresholds for cardinal compared to oblique directions. For each subject, we also estimated MAE tuning width for a cardinal and an oblique direction by measuring the strength of the MAE for adapter stimuli containing different directional variances. The MAE tuning width was smaller for the cardinal direction, suggesting a fundamental similarity between motion direction discrimination and tuning of the MAE. We constructed a model of encoding of motion stimuli by V1 and MT and decoding of stimulus information from the cells in area MT. The model includes an anisotropy in the representation of different directions of motion in area V1. As a consequence of the connections implemented in the model, this anisotropy propagates to cells in MT. Model simulations predicted an oblique effect for both direction discrimination thresholds and MAE tuning width, consistent with our experimental results. The model also concurs with a recent report that the magnitude of the oblique effect for direction discrimination is inversely proportional to the directional variance of the stimulus. The agreement between model predictions and empirical data was obtained only when the model employed a maximum likelihood decoding algorithm. Alternative decoding mechanisms such as vector averaging and winner-take-all failed to account for the psychophysical results.

[1]  Shaowen Bao,et al.  Early experience impairs perceptual discrimination , 2007, Nature Neuroscience.

[2]  Katsumi Aoki,et al.  Recent development of flow visualization , 2004, J. Vis..

[3]  D. Perrett,et al.  The `Ideal Homunculus': decoding neural population signals , 1998, Trends in Neurosciences.

[4]  Robert A Jacobs,et al.  Bayesian integration of visual and auditory signals for spatial localization. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[5]  R. L. Valois,et al.  The orientation and direction selectivity of cells in macaque visual cortex , 1982, Vision Research.

[6]  R. Freeman,et al.  Oblique effect: a neural basis in the visual cortex. , 2003, Journal of neurophysiology.

[7]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[8]  Q. Zaidi,et al.  Fundamental Failures of Shape Constancy Resulting from Cortical Anisotropy , 2007, The Journal of Neuroscience.

[9]  R Blake,et al.  Another perspective on the visual motion aftereffect. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[10]  A. Pouget,et al.  Reading population codes: a neural implementation of ideal observers , 1999, Nature Neuroscience.

[11]  R. Freeman,et al.  The Derivation of Direction Selectivity in the Striate Cortex , 2004, The Journal of Neuroscience.

[12]  J. Gold,et al.  Neural computations that underlie decisions about sensory stimuli , 2001, Trends in Cognitive Sciences.

[13]  H. Ross,et al.  Genetic and Environmental Factors in Orientation Anisotropy: A Field Study in the British Isles , 1979, Perception.

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

[15]  J. Movshon,et al.  Motion Integration by Neurons in Macaque MT Is Local, Not Global , 2007, The Journal of Neuroscience.

[16]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

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

[18]  C. Furmanski,et al.  Learning Strengthens the Response of Primary Visual Cortex to Simple Patterns , 2004, Current Biology.

[19]  Shaowen Bao,et al.  Distributed representation of perceptual categories in the auditory cortex , 2008, Journal of Computational Neuroscience.

[20]  Frans A. J. Verstraten,et al.  The motion aftereffect , 1998, Trends in Cognitive Sciences.

[21]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[22]  A. Watson Probability summation over time , 1979, Vision Research.

[23]  B. L. Gros,et al.  Anisotropies in visual motion perception: a fresh look. , 1998, Journal of the Optical Society of America. A, Optics, image science, and vision.

[24]  B N Timney,et al.  Orientation anisotropy: incidence and magnitude in Caucasian and Chinese subjects. , 1976, Science.

[25]  Vivien A. Casagrande,et al.  Unequal representation of cardinal vs. oblique orientations in the middle temporal visual area , 2006, Proceedings of the National Academy of Sciences.

[26]  G. Westheimer Meridional anisotropy in visual processing: implications for the neural site of the oblique effect , 2003, Vision Research.

[27]  S. Appelle Perception and discrimination as a function of stimulus orientation: the "oblique effect" in man and animals. , 1972, Psychological bulletin.

[28]  Steven C Dakin,et al.  An oblique effect for local motion: psychophysics and natural movie statistics. , 2005, Journal of vision.

[29]  H Sompolinsky,et al.  Simple models for reading neuronal population codes. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Anthony J. Movshon,et al.  Optimal representation of sensory information by neural populations , 2006, Nature Neuroscience.

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

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

[33]  William T Newsome,et al.  Middle Temporal Visual Area Microstimulation Influences Veridical Judgments of Motion Direction , 2002, The Journal of Neuroscience.

[34]  Margaret S Livingstone,et al.  End-Stopping and the Aperture Problem Two-Dimensional Motion Signals in Macaque V1 , 2003, Neuron.

[35]  Y. J. Tejwani,et al.  Robot vision , 1989, IEEE International Symposium on Circuits and Systems,.

[36]  A. Watson,et al.  Quest: A Bayesian adaptive psychometric method , 1983, Perception & psychophysics.

[37]  D. Heeger,et al.  Neuronal Basis of the Motion Aftereffect Reconsidered , 2001, Neuron.

[38]  R. Blake,et al.  Another means for measuring the motion aftereffect , 1993, Vision Research.

[39]  R. Sekuler,et al.  A specific and enduring improvement in visual motion discrimination. , 1982, Science.

[40]  H. Barlow,et al.  Evidence for a Physiological Explanation of the Waterfall Phenomenon and Figural After-effects , 1963, Nature.

[41]  Xiangmin Xu,et al.  How do functional maps in primary visual cortex vary with eccentricity? , 2007, The Journal of comparative neurology.

[42]  J. Patel,et al.  Handbook of the normal distribution , 1983 .

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

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

[45]  C D Salzman,et al.  Neural mechanisms for forming a perceptual decision. , 1994, Science.

[46]  O. Braddick,et al.  Integration across Directions in Dynamic Random Dot Displays: Vector Summation or Winner Take All? , 1996, Vision Research.

[47]  Stephen G. Lisberger,et al.  Directional Anisotropies Reveal a Functional Segregation of Visual Motion Processing for Perception and Action , 2003, Neuron.

[48]  S. Petersen,et al.  Direction-specific adaptation in area MT of the owl monkey , 1985, Brain Research.

[49]  J. Movshon,et al.  Integration of sensory evidence in motion discrimination. , 2007, Journal of vision.

[50]  C. Furmanski,et al.  An oblique effect in human primary visual cortex , 2000, Nature Neuroscience.

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