Two distinct types of remapping in primate cortical area V4

Visual neurons typically receive information from a limited portion of the retina, and such receptive fields are a key organizing principle for much of visual cortex. At the same time, there is strong evidence that receptive fields transiently shift around the time of saccades. The nature of the shift is controversial: Previous studies have found shifts consistent with a role for perceptual constancy; other studies suggest a role in the allocation of spatial attention. Here we present evidence that both the previously documented functions exist in individual neurons in primate cortical area V4. Remapping associated with perceptual constancy occurs for saccades in all directions, while attentional shifts mainly occur for neurons with receptive fields in the same hemifield as the saccade end point. The latter are relatively sluggish and can be observed even during saccade planning. Overall these results suggest a complex interplay of visual and extraretinal influences during the execution of saccades.

[1]  P. Cavanagh,et al.  Visual stability based on remapping of attention pointers , 2010, Trends in Cognitive Sciences.

[2]  R. Quian Quiroga,et al.  Unsupervised Spike Detection and Sorting with Wavelets and Superparamagnetic Clustering , 2004, Neural Computation.

[3]  Patrick Cavanagh,et al.  Allocation of attention across saccades. , 2013, Journal of neurophysiology.

[4]  H. Deubel The time course of presaccadic attention shifts , 2008, Psychological research.

[5]  James W Bisley,et al.  A Lack of Anticipatory Remapping of Retinotopic Receptive Fields in the Middle Temporal Area , 2011, The Journal of Neuroscience.

[6]  T. Moore,et al.  Saccades and shifting receptive fields: anticipating consequences or selecting targets? , 2014, Trends in Cognitive Sciences.

[7]  Robert H. Wurtz,et al.  Influence of the thalamus on spatial visual processing in frontal cortex , 2006, Nature.

[8]  C. Connor,et al.  Responses to contour features in macaque area V4. , 1999, Journal of neurophysiology.

[9]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. II. Memory responses. , 2001, Journal of neurophysiology.

[10]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[11]  T. Wiesel,et al.  Functional architecture of macaque monkey visual cortex , 1977 .

[12]  Nicholas A. Steinmetz,et al.  Visual Space is Compressed in Prefrontal Cortex Before Eye Movements , 2014, Nature.

[13]  Tirin Moore,et al.  Changes in Visual Receptive Fields with Microstimulation of Frontal Cortex , 2006, Neuron.

[14]  C. Colby,et al.  Spatial updating in area LIP is independent of saccade direction. , 2006, Journal of neurophysiology.

[15]  Jude F. Mitchell,et al.  Attention Influences Single Unit and Local Field Potential Response Latencies in Visual Cortical Area V4 , 2012, The Journal of Neuroscience.

[16]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[17]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[18]  D. V. van Essen,et al.  Responses in area V4 depend on the spatial relationship between stimulus and attention. , 1996, Journal of neurophysiology.

[19]  Nicholas A. Steinmetz,et al.  Eye Movement Preparation Modulates Neuronal Responses in Area V4 When Dissociated from Attentional Demands , 2014, Neuron.

[20]  I. Ial,et al.  Nature Communications , 2010, Nature Cell Biology.

[21]  Theodoros P. Zanos,et al.  Removal of spurious correlations between spikes and local field potentials. , 2011, Journal of neurophysiology.

[22]  Christopher C. Pack,et al.  Context dependence of receptive field remapping in superior colliculus. , 2011, Journal of neurophysiology.

[23]  Daniel Guitton,et al.  Perisaccadic Remapping and Rescaling of Visual Responses in Macaque Superior Colliculus , 2012, PloS one.

[24]  P. Cavanagh,et al.  Predictive remapping of attention across eye movements , 2011, Nature Neuroscience.

[25]  Carol L Colby,et al.  Shape selectivity and remapping in dorsal stream visual area LIP. , 2014, Journal of neurophysiology.

[26]  Christopher C. Pack,et al.  The Geometry of Perisaccadic Visual Perception , 2009, The Journal of Neuroscience.

[27]  L. Matin,et al.  Visual Perception of Direction for Stimuli Flashed During Voluntary Saccadic Eye Movements , 1965, Science.

[28]  B. Fischer,et al.  Selection of visual targets activates prelunate cortical cells in trained rhesus monkey , 2004, Experimental Brain Research.

[29]  M. Goldberg,et al.  Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. , 1995, Journal of neurophysiology.

[30]  E. J. Tehovnik,et al.  Eye Movements Modulate Visual Receptive Fields of V4 Neurons , 2001, Neuron.

[31]  Frank Bremmer,et al.  Neural Correlates of Visual Localization and Perisaccadic Mislocalization , 2003, Neuron.

[32]  Robert Desimone,et al.  Cortical connections of area V4 in the macaque. , 2000, Cerebral cortex.

[33]  H. Deubel,et al.  Saccade target selection and object recognition: Evidence for a common attentional mechanism , 1996, Vision Research.

[34]  David C. Burr,et al.  Compression of visual space before saccades , 1997, Nature.

[35]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[36]  Robert Desimone,et al.  Lesions of prefrontal cortex reduce attentional modulation of neuronal responses and synchrony in V4 , 2014, Nature Neuroscience.

[37]  C. Gross,et al.  Visuotopic organization and extent of V3 and V4 of the macaque , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

[39]  D. V. van Essen,et al.  Spatial Attention Effects in Macaque Area V4 , 1997, The Journal of Neuroscience.

[40]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. I. Predictive visual responses. , 1997, Journal of neurophysiology.

[41]  Theodoros P. Zanos,et al.  A Sensorimotor Role for Traveling Waves in Primate Visual Cortex , 2015, Neuron.

[42]  Anirvan S. Nandy,et al.  The Fine Structure of Shape Tuning in Area V4 , 2013, Neuron.

[43]  M. Goldberg,et al.  The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey. , 2003, Journal of neurophysiology.

[44]  Theodoros P. Zanos,et al.  Local field potentials reflect multiple spatial scales in V4 , 2013, Front. Comput. Neurosci..

[45]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

[46]  R. Wurtz,et al.  A Pathway in Primate Brain for Internal Monitoring of Movements , 2002, Science.

[47]  Jan Churan,et al.  Perceptual compression of visual space during eye-head gaze shifts. , 2011, Journal of vision.

[48]  Kae Nakamura,et al.  Updating of the visual representation in monkey striate and extrastriate cortex during saccades , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  S. Zeki The representation of colours in the cerebral cortex , 1980, Nature.

[50]  Yali Amit,et al.  Single-unit stability using chronically implanted multielectrode arrays. , 2009, Journal of neurophysiology.

[51]  A. Huberman,et al.  Architecture and Activity-Mediated Refinement of Axonal Projections from a Mosaic of Genetically Identified Retinal Ganglion Cells , 2008, Neuron.

[52]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[53]  Robert H Wurtz,et al.  Modulation of shifting receptive field activity in frontal eye field by visual salience. , 2011, Journal of neurophysiology.

[54]  Marcus Kaiser,et al.  Perisaccadic Mislocalization Orthogonal to Saccade Direction , 2004, Neuron.

[55]  Kenji Kawano,et al.  Neurons in cortical area MST remap the memory trace of visual motion across saccadic eye movements , 2014, Proceedings of the National Academy of Sciences.

[56]  Bevil R. Conway,et al.  Toward a Unified Theory of Visual Area V4 , 2012, Neuron.

[57]  R. Wurtz Neuronal mechanisms of visual stability , 2008, Vision Research.

[58]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[59]  R. Desimone,et al.  The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4 , 2008, The Journal of Neuroscience.