Compound Stimuli Reveal the Structure of Visual Motion Selectivity in Macaque MT Neurons

Abstract Motion selectivity in primary visual cortex (V1) is approximately separable in orientation, spatial frequency, and temporal frequency (“frequency-separable”). Models for area MT neurons posit that their selectivity arises by combining direction-selective V1 afferents whose tuning is organized around a tilted plane in the frequency domain, specifying a particular direction and speed (“velocity-separable”). This construction explains “pattern direction-selective” MT neurons, which are velocity-selective but relatively invariant to spatial structure, including spatial frequency, texture and shape. We designed a set of experiments to distinguish frequency-separable and velocity-separable models and executed them with single-unit recordings in macaque V1 and MT. Surprisingly, when tested with single drifting gratings, most MT neurons’ responses are fit equally well by models with either form of separability. However, responses to plaids (sums of two moving gratings) tend to be better described as velocity-separable, especially for pattern neurons. We conclude that direction selectivity in MT is primarily computed by summing V1 afferents, but pattern-invariant velocity tuning for complex stimuli may arise from local, recurrent interactions.

[1]  Alexander S. Ecker,et al.  Neural system identification for large populations separating "what" and "where" , 2017, NIPS.

[2]  I. Ohzawa,et al.  Subspace mapping of the three-dimensional spectral receptive field of macaque MT neurons. , 2016, Journal of neurophysiology.

[3]  James A. Bednar,et al.  Model Constrained by Visual Hierarchy Improves Prediction of Neural Responses to Natural Scenes , 2016, PLoS Comput. Biol..

[4]  J Anthony Movshon,et al.  Properties of pattern and component direction-selective cells in area MT of the macaque. , 2016, Journal of neurophysiology.

[5]  Yale E. Cohen,et al.  Recent refinements to cranial implants for rhesus macaques (Macaca mulatta) , 2016, Lab Animal.

[6]  Xin Huang,et al.  Distributed and Dynamic Neural Encoding of Multiple Motion Directions of Transparently Moving Stimuli in Cortical Area MT , 2015, The Journal of Neuroscience.

[7]  Eero P. Simoncelli,et al.  Origin and Function of Tuning Diversity in Macaque Visual Cortex , 2015, Neuron.

[8]  D. R. Muir,et al.  Functional organization of excitatory synaptic strength in primary visual cortex , 2015, Nature.

[9]  Adolf Wohlgemuth,et al.  On the after-effect of seen movement , 2015 .

[10]  Eero P. Simoncelli,et al.  Partitioning neuronal variability , 2014, Nature Neuroscience.

[11]  Selina S. Solomon,et al.  Integration and segregation of multiple motion signals by neurons in area MT of primate. , 2014, Journal of neurophysiology.

[12]  T. Uka,et al.  Responses to Random Dot Motion Reveal Prevalence of Pattern-Motion Selectivity in Area MT , 2013, The Journal of Neuroscience.

[13]  Chris Tailby,et al.  Visual motion integration by neurons in the middle temporal area of a New World monkey, the marmoset , 2011, The Journal of physiology.

[14]  J. Gallant,et al.  A Three-Dimensional Spatiotemporal Receptive Field Model Explains Responses of Area MT Neurons to Naturalistic Movies , 2011, The Journal of Neuroscience.

[15]  J. M. Parker,et al.  A watertight acrylic-free titanium recording chamber for electrophysiology in behaving monkeys. , 2011, Journal of neurophysiology.

[16]  D. L. Adams,et al.  A biocompatible titanium headpost for stabilizing behaving monkeys. , 2007, Journal of neurophysiology.

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

[18]  Nicholas J. Priebe,et al.  Tuning for Spatiotemporal Frequency and Speed in Directionally Selective Neurons of Macaque Striate Cortex , 2006, The Journal of Neuroscience.

[19]  J. Movshon,et al.  Dynamics of motion signaling by neurons in macaque area MT , 2005, Nature Neuroscience.

[20]  John A. Perrone,et al.  A visual motion sensor based on the properties of V1 and MT neurons , 2004, Vision Research.

[21]  Nicholas J. Priebe,et al.  The Neural Representation of Speed in Macaque Area MT/V5 , 2003, The Journal of Neuroscience.

[22]  K. H. Britten,et al.  Contrast dependence of response normalization in area MT of the rhesus macaque. , 2002, Journal of neurophysiology.

[23]  J. Movshon,et al.  Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[24]  Alexander Thiele,et al.  A model of speed tuning in MT neurons , 2002, Vision Research.

[25]  Alexander Thiele,et al.  Speed skills: measuring the visual speed analyzing properties of primate MT neurons , 2001, Nature Neuroscience.

[26]  Christopher C. Pack,et al.  Temporal dynamics of a neural solution to the aperture problem in visual area MT of macaque brain , 2001, Nature.

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

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

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

[30]  Dejan Todorović,et al.  A Gem from the Past: Pleikart Stumpf's (1911) Anticipation of the Aperture Problem, Reichardt Detectors, and Perceived Motion Loss at Equiluminance , 1996 .

[31]  R. Shapley,et al.  Temporal-frequency selectivity in monkey visual cortex , 1996, Visual Neuroscience.

[32]  R. Reid,et al.  Specificity of monosynaptic connections from thalamus to visual cortex , 1995, Nature.

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

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

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

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

[37]  C. Enroth-Cugell,et al.  Spatio‐temporal interactions in cat retinal ganglion cells showing linear spatial summation. , 1983, The Journal of physiology.

[38]  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.

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

[40]  John H. R. Maunsell,et al.  The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization , 1981, The Journal of comparative neurology.

[41]  D Marr,et al.  Directional selectivity and its use in early visual processing , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[42]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of striate cortical neurones , 1975, Nature.

[43]  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.

[44]  Hans Wallach Über visuell wahrgenommene Bewegungsrichtung , 1935 .

[45]  Yadin Dudai,et al.  Cognitive Architectures , 2015, Neuron.

[46]  A Look at Motion in the Frequency Domain , 2010 .

[47]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[48]  Paul R. Schrater,et al.  Mechanisms of visual motion detection , 2000, Nature Neuroscience.

[49]  P. Stumpf A gem from the past: Pleikart Stumpf's (1911) anticipation of the aperture problem, Reichardt detectors, and perceived motion loss at equiluminance. , 1996, Perception.

[50]  Robert Tibshirani,et al.  An Introduction to the Bootstrap CHAPMAN & HALL/CRC , 1993 .

[51]  E. Adelson,et al.  THE ANALYSIS OF MOVING VISUAL PATTERNS , 1997 .