Dynamics of Population Response to Changes of Motion Direction in Primary Visual Cortex

The visual system is thought to represent the direction of moving objects in the relative activity of large populations of cortical neurons that are broadly tuned to the direction of stimulus motion, but how changes in the direction of a moving stimulus are represented in the population response remains poorly understood. Here we take advantage of the orderly mapping of direction selectivity in ferret primary visual cortex (V1) to explore how abrupt changes in the direction of a moving stimulus are encoded in population activity using voltage-sensitive dye imaging. For stimuli moving in a constant direction, the peak of the V1 population response accurately represented the direction of stimulus motion, but following abrupt changes in motion direction, the peak transiently departed from the direction of stimulus motion in a fashion that varied with the direction offset angle and was well predicted from the response to the component directions. We conclude that cortical dynamics and population coding mechanisms combine to place constraints on the accuracy with which abrupt changes in direction of motion can be represented by cortical circuits.

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

[2]  A. Kohn.  Visual adaptation: physiology, mechanisms, and functional benefits. , 2007, Journal of neurophysiology.

[3]  A. Grinvald,et al.  Functional Organization for Direction of Motion and Its Relationship to Orientation Maps in Cat Area 18 , 1996, The Journal of Neuroscience.

[4]  F. Chavane,et al.  Cortical response field dynamics in cat visual cortex. , 2007, Cerebral cortex.

[5]  A. Grinvald,et al.  Dynamics and Constancy in Cortical Spatiotemporal Patterns of Orientation Processing , 2002, Science.

[6]  Matteo Carandini,et al.  Coding of stimulus sequences by population responses in visual cortex , 2009, Nature Neuroscience.

[7]  Henry J. Alitto,et al.  Orientation tuning, but not direction selectivity, is invariant to temporal frequency in primary visual cortex. , 2005, Journal of neurophysiology.

[8]  F. A. Geldard,et al.  The Cutaneous "Rabbit": A Perceptual Illusion , 1972, Science.

[9]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[10]  Roger N. Shepard,et al.  Spatio-temporal probing of apparent rotational movement , 1977 .

[11]  M. Sur,et al.  Adaptation-Induced Plasticity of Orientation Tuning in Adult Visual Cortex , 2000, Neuron.

[12]  E. Miller,et al.  Dynamics of neuronal sensitivity in visual cortex and local feature discrimination , 2002, Nature Neuroscience.

[13]  D. Fitzpatrick,et al.  The development of direction selectivity in ferret visual cortex requires early visual experience , 2006, Nature Neuroscience.

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

[15]  Justin L. Gardner,et al.  A Population Decoding Framework for Motion Aftereffects on Smooth Pursuit Eye Movements , 2004, The Journal of Neuroscience.

[16]  M. Wertheimer.  Experimental studies on the seeing of motion , 1961 .

[17]  N. Suga.  Perceptual Illusion of Rotation of Three-Dimensional Objects , 2022 .

[18]  Stefan Treue,et al.  Seeing multiple directions of motion—physiology and psychophysics , 2000, Nature Neuroscience.

[19]  B R Payne,et al.  Organization of orientation and direction selectivity in areas 17 and 18 of cat cerebral cortex. , 1987, Journal of neurophysiology.

[20]  Stephane Molotchnikoff,et al.  Visual Cells Remember Earlier Applied Target: Plasticity of Orientation Selectivity , 2008, PloS one.

[21]  B L Finlay,et al.  Quantitative studies of single-cell properties in monkey striate cortex. IV. Corticotectal cells. , 1976, Journal of neurophysiology.

[22]  Srimant P Tripathy,et al.  Misperceptions of Trajectories of Dots Moving through the Blind Spot , 2006, Perception.

[23]  R. Vautin,et al.  Responses of single cells in cat visual cortex to prolonged stimulus movement: neural correlates of visual aftereffects. , 1977, Journal of neurophysiology.

[25]  Yang Dan,et al.  Dynamic Modification of Cortical Orientation Tuning Mediated by Recurrent Connections , 2002, Neuron.

[26]  Amiram Grinvald,et al.  VSDI: a new era in functional imaging of cortical dynamics , 2004, Nature Reviews Neuroscience.

[27]  Debashis Kushary,et al.  Bootstrap Methods and Their Application , 2000, Technometrics.

[28]  Leonard E. White,et al.  Mapping multiple features in the population response of visual cortex , 2003, Nature.

[29]  A. Grinvald,et al.  Imaging Cortical Dynamics at High Spatial and Temporal Resolution with Novel Blue Voltage-Sensitive Dyes , 1999, Neuron.

[30]  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.

[31]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[32]  F. Chavane,et al.  Imaging cortical correlates of illusion in early visual cortex , 2004, Nature.

[33]  R. Shepard,et al.  Perceptual illusion of rotation of three-dimensional objects. , 1976, Science.

[34]  J. Movshon,et al.  Pattern adaptation and cross-orientation interactions in the primary visual cortex , 1998, Neuropharmacology.

[35]  P. Lennie,et al.  Rapid adaptation in visual cortex to the structure of images. , 1999, Science.

[36]  D. Fitzpatrick,et al.  A systematic map of direction preference in primary visual cortex , 1996, Nature.

[37]  Nicholas J. Priebe,et al.  Constraints on the source of short-term motion adaptation in macaque area MT. II. tuning of neural circuit mechanisms. , 2002, Journal of neurophysiology.

[38]  A. Grinvald,et al.  Real-time optical imaging of naturally evoked electrical activity in intact frog brain , 1984, Nature.