Functional Characterization of the Extraclassical Receptive Field in Macaque V1: Contrast, Orientation, and Temporal Dynamics

Neurons in primary visual cortex, V1, very often have extraclassical receptive fields (eCRFs). The eCRF is defined as the region of visual space where stimuli cannot elicit a spiking response but can modulate the response of a stimulus in the classical receptive field (CRF). We investigated the dependence of the eCRF on stimulus contrast and orientation in macaque V1 cells for which the laminar location was determined. The eCRF was more sensitive to contrast than the CRF across the whole population of V1 cells with the greatest contrast differential in layer 2/3. We confirmed that many V1 cells experience stronger suppression for collinear than orthogonal stimuli in the eCRF. Laminar analysis revealed that the predominant bias for collinear suppression was found in layers 2/3 and 4b. The laminar pattern of contrast and orientation dependence suggests that eCRF suppression may derive from different neural circuits in different layers, and may be comprised of two distinct components: orientation-tuned and untuned suppression. On average tuned suppression was delayed by ∼25 ms compared with the onset of untuned suppression. Therefore, response modulation by the eCRF develops dynamically and rapidly in time.

[1]  K. Naka,et al.  S‐potentials from luminosity units in the retina of fish (Cyprinidae) , 1966, The Journal of physiology.

[2]  Hans Supèr,et al.  Feed-Forward Segmentation of Figure-Ground and Assignment of Border-Ownership , 2010, PloS one.

[3]  C. Gilbert,et al.  Contour Saliency in Primary Visual Cortex , 2006, Neuron.

[4]  P. Lennie,et al.  The Impact of Suppressive Surrounds on Chromatic Properties of Cortical Neurons , 2004, The Journal of Neuroscience.

[5]  Dario L Ringach,et al.  Untuned Suppression Makes a Major Contribution to the Enhancement of Orientation Selectivity in Macaque V1 , 2011, The Journal of Neuroscience.

[6]  E. Todorov,et al.  A local circuit approach to understanding integration of long-range inputs in primary visual cortex. , 1998, Cerebral cortex.

[7]  Victor A. F. Lamme.  The neurophysiology of figure-ground segregation in primary visual cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  C. Blakemore,et al.  Lateral inhibition between orientation detectors in the cat's visual cortex , 2004, Experimental Brain Research.

[9]  J. B. Levitt,et al.  Comparison of Spatial Summation Properties of Neurons in Macaque V1 and V2 , 2009, Journal of neurophysiology.

[10]  M. Hawken,et al.  Laminar organization and contrast sensitivity of direction-selective cells in the striate cortex of the Old World monkey , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[12]  R. Shapley,et al.  Visual spatial characterization of macaque V1 neurons. , 2001, Journal of neurophysiology.

[13]  Branka Spehar,et al.  Dynamics of collinear contrast facilitation are consistent with long-range horizontal striate transmission , 2005, Vision Research.

[14]  W. Martin Usrey,et al.  Origin and Dynamics of Extraclassical Suppression in the Lateral Geniculate Nucleus of the Macaque Monkey , 2008, Neuron.

[15]  J. Gallant,et al.  Natural Stimulation of the Nonclassical Receptive Field Increases Information Transmission Efficiency in V1 , 2002, The Journal of Neuroscience.

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

[17]  C. Gilbert,et al.  Spatial distribution of contextual interactions in primary visual cortex and in visual perception. , 2000, Journal of neurophysiology.

[18]  R. Shapley,et al.  Effect of stimulus size on the dynamics of orientation selectivity in Macaque V1. , 2005, Journal of neurophysiology.

[19]  K. Obermayer,et al.  The Role of Feedback in Shaping the Extra-Classical Receptive Field of Cortical Neurons: A Recurrent Network Model , 2006, The Journal of Neuroscience.

[20]  H. Jones,et al.  Visual cortical mechanisms detecting focal orientation discontinuities , 1995, Nature.

[21]  Erich W. Graf,et al.  Contextual effects in speed perception may occur at an early stage of processing , 2010, Vision Research.

[22]  J. Movshon,et al.  Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[23]  P. Lennie,et al.  Early and Late Mechanisms of Surround Suppression in Striate Cortex of Macaque , 2005, The Journal of Neuroscience.

[24]  I. Ohzawa,et al.  Length and width tuning of neurons in the cat's primary visual cortex. , 1994, Journal of neurophysiology.

[25]  C. Blakemore,et al.  Characteristics of surround inhibition in cat area 17 , 1997, Experimental Brain Research.

[26]  Evan S. Schaffer,et al.  Inhibitory Stabilization of the Cortical Network Underlies Visual Surround Suppression , 2009, Neuron.

[27]  D. Hubel,et al.  Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. , 1966, Journal of neurophysiology.

[28]  A. Ainsworth,et al.  Glass-coated platinum-plated tungsten microelectrodes , 1972, Medical and biological engineering.

[29]  U. Polat,et al.  Collinear stimuli regulate visual responses depending on cell's contrast threshold , 1998, Nature.

[30]  R. Shapley,et al.  Contrast's effect on spatial summation by macaque V1 neurons , 1999, Nature Neuroscience.

[31]  Paul R. Martin,et al.  Extraclassical Receptive Field Properties of Parvocellular, Magnocellular, and Koniocellular Cells in the Primate Lateral Geniculate Nucleus , 2002, The Journal of Neuroscience.

[32]  R. Shapley,et al.  The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[33]  R. von der Heydt,et al.  Analysis of the Context Integration Mechanisms Underlying Figure–Ground Organization in the Visual Cortex , 2010, The Journal of Neuroscience.

[34]  D. Tolhurst,et al.  Calculating the contrasts that retinal ganglion cells and LGN neurones encounter in natural scenes , 2000, Vision Research.

[35]  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.

[36]  J. Movshon,et al.  Time Course and Time-Distance Relationships for Surround Suppression in Macaque V1 Neurons , 2003, The Journal of Neuroscience.

[37]  Alessandra Angelucci,et al.  Contrast-dependence of surround suppression in Macaque V1: Experimental testing of a recurrent network model , 2010, NeuroImage.

[38]  Edward M Callaway,et al.  Visual spatial summation in macaque geniculocortical afferents. , 2006, Journal of neurophysiology.

[39]  Alessandra Angelucci,et al.  Strong Recurrent Networks Compute the Orientation Tuning of Surround Modulation in the Primate Primary Visual Cortex , 2012, The Journal of Neuroscience.

[40]  G Westheimer,et al.  Dynamics of spatial summation in primary visual cortex of alert monkeys. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[41]  D. Tolhurst,et al.  Coding of the contrasts in natural images by populations of neurons in primary visual cortex (V1) , 2003, Vision Research.

[42]  Arash Yazdanbakhsh,et al.  End stopping in V1 is sensitive to contrast , 2006, Nature Neuroscience.

[43]  Alessandra Angelucci,et al.  Different Orientation Tuning of Near- and Far-Surround Suppression in Macaque Primary Visual Cortex Mirrors Their Tuning in Human Perception , 2013, The Journal of Neuroscience.

[44]  Frances S. Chance,et al.  Gain modulation of neuronal responses by subtractive and divisive mechanisms of inhibition. , 2009, Journal of neurophysiology.

[45]  R. Shapley,et al.  Orientation Selectivity in Macaque V1: Diversity and Laminar Dependence , 2002, The Journal of Neuroscience.

[46]  A. B. Bonds.  Temporal dynamics of contrast gain in single cells of the cat striate cortex , 1991, Visual Neuroscience.

[47]  J. Movshon,et al.  Dynamics of Suppression in Macaque Primary Visual Cortex , 2006, The Journal of Neuroscience.

[48]  R. Shapley,et al.  Dynamics of orientation tuning in macaque V1: the role of global and tuned suppression. , 2003, Journal of neurophysiology.

[49]  P. Lennie,et al.  Local signals from beyond the receptive fields of striate cortical neurons. , 2003, Journal of neurophysiology.

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

[51]  H. Spekreijse,et al.  Two distinct modes of sensory processing observed in monkey primary visual cortex (V1) , 2001, Nature Neuroscience.

[52]  C. Gilbert.  Laminar differences in receptive field properties of cells in cat primary visual cortex , 1977, The Journal of physiology.

[53]  J. B. Levitt,et al.  Contrast dependence of contextual effects in primate visual cortex , 1997, nature.

[54]  Tomoyuki Naito,et al.  Contrast‐dependent, contextual response modulation in primary visual cortex and lateral geniculate nucleus of the cat , 2006, The European journal of neuroscience.

[55]  L. Schwabe,et al.  Response facilitation from the "suppressive" receptive field surround of macaque V1 neurons. , 2007, Journal of neurophysiology.

[56]  Robert Shapley,et al.  Correlation of local and global orientation and spatial frequency tuning in macaque V1 , 2004, The Journal of physiology.

[57]  J. B. Levitt,et al.  The spatial extent over which neurons in macaque striate cortex pool visual signals , 2002, Visual Neuroscience.

[58]  B. Richmond,et al.  Latency: another potential code for feature binding in striate cortex. , 1996, Journal of neurophysiology.

[59]  H. Ozeki,et al.  Relationship between Excitation and Inhibition Underlying Size Tuning and Contextual Response Modulation in the Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.