Spatiotopic perceptual learning mediated by retinotopic processing and attentional remapping

Visual processing takes place in both retinotopic and spatiotopic frames of reference. Whereas visual perceptual learning is usually specific to the trained retinotopic location, our recent study has shown spatiotopic specificity of learning in motion direction discrimination. To explore the mechanisms underlying spatiotopic processing and learning, and to examine whether similar mechanisms also exist in visual form processing, we trained human subjects to discriminate an orientation difference between two successively displayed stimuli, with a gaze shift in between to manipulate their positional relation in the spatiotopic frame of reference without changing their retinal locations. Training resulted in better orientation discriminability for the trained than for the untrained spatial relation of the two stimuli. This learning‐induced spatiotopic preference was seen only at the trained retinal location and orientation, suggesting experience‐dependent spatiotopic form processing directly based on a retinotopic map. Moreover, a similar but weaker learning‐induced spatiotopic preference was still present even if the first stimulus was rendered irrelevant to the orientation discrimination task by having the subjects judge the orientation of the second stimulus relative to its mean orientation in a block of trials. However, if the first stimulus was absent, and thus no attention was captured before the gaze shift, the learning produced no significant spatiotopic preference, suggesting an important role of attentional remapping in spatiotopic processing and learning. Taken together, our results suggest that spatiotopic visual representation can be mediated by interactions between retinotopic processing and attentional remapping, and can be modified by perceptual training.

[1]  P. P. Battaglini,et al.  Parietal neurons encoding spatial locations in craniotopic coordinates , 2004, Experimental Brain Research.

[2]  Julie D. Golomb,et al.  Robustness of the retinotopic attentional trace after eye movements. , 2010, Journal of vision.

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

[4]  Emilio Salinas,et al.  Gain Modulation A Major Computational Principle of the Central Nervous System , 2000, Neuron.

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

[6]  P. Wenderoth,et al.  Retinotopic encoding of the direction aftereffect , 2008, Vision Research.

[7]  Patrick Cavanagh,et al.  The reference frame of the motion aftereffect is retinotopic. , 2009, Journal of vision.

[8]  Michael E. Goldberg,et al.  The Postsaccadic Unreliability of Gain Fields Renders It Unlikely that the Motor System Can Use Them to Calculate Target Position in Space , 2012, Neuron.

[9]  Michael H. Herzog,et al.  Nonretinotopic Exogenous Attention , 2011, Current Biology.

[10]  K. Hoffmann,et al.  Eye position effects in monkey cortex. I. Visual and pursuit-related activity in extrastriate areas MT and MST. , 1997, Journal of neurophysiology.

[11]  Richard A. Andersen,et al.  A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons , 1988, Nature.

[12]  Takeo Watanabe,et al.  Advances in visual perceptual learning and plasticity , 2010, Nature Reviews Neuroscience.

[13]  Jan Theeuwes,et al.  Evidence for the predictive remapping of visual attention , 2009, Experimental Brain Research.

[14]  R. M. Siegel,et al.  Encoding of spatial location by posterior parietal neurons. , 1985, Science.

[15]  A. Fiorentini,et al.  Perceptual learning specific for orientation and spatial frequency , 1980, Nature.

[16]  Jan Theeuwes,et al.  A Retinotopic Attentional Trace after Saccadic Eye Movements: Evidence from Event-related Potentials , 2013, Journal of Cognitive Neuroscience.

[17]  D. Melcher Spatiotopic Transfer of Visual-Form Adaptation across Saccadic Eye Movements , 2005, Current Biology.

[18]  Wu Li,et al.  Perceptual learning beyond retinotopic reference frame , 2010, Proceedings of the National Academy of Sciences.

[19]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[20]  R. Andersen Encoding of intention and spatial location in the posterior parietal cortex. , 1995, Cerebral cortex.

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

[22]  G. Orban,et al.  Human perceptual learning in identifying the oblique orientation: retinotopy, orientation specificity and monocularity. , 1995, The Journal of physiology.

[23]  S. Klein,et al.  Rule-Based Learning Explains Visual Perceptual Learning and Its Specificity and Transfer , 2010, The Journal of Neuroscience.

[24]  Patrick Cavanagh,et al.  Remapped visual masking. , 2011, Journal of vision.

[25]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

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

[27]  H. Pashler,et al.  Improvement in line orientation discrimination is retinally local but dependent on cognitive set , 1992, Perception & psychophysics.

[28]  R. M. Siegel,et al.  Maps of Visual Space in Human Occipital Cortex Are Retinotopic, Not Spatiotopic , 2008, The Journal of Neuroscience.

[29]  D. Sagi,et al.  Generalized Perceptual Learning in the Absence of Sensory Adaptation , 2012, Current Biology.

[30]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[31]  F. Bremmer,et al.  Spatial invariance of visual receptive fields in parietal cortex neurons , 1997, Nature.

[32]  S. Celebrini,et al.  Gaze direction controls response gain in primary visual-cortex neurons , 1999, Nature.

[33]  D Sagi,et al.  Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Julie D. Golomb,et al.  Attentional Facilitation throughout Human Visual Cortex Lingers in Retinotopic Coordinates after Eye Movements , 2010, The Journal of Neuroscience.

[35]  Julie D. Golomb,et al.  Attention doesn’t slide: spatiotopic updating after eye movements instantiates a new, discrete attentional locus , 2011, Attention, perception & psychophysics.

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

[37]  David Burr,et al.  Spatiotopic perceptual maps in humans: evidence from motion adaptation , 2012, Proceedings of the Royal Society B: Biological Sciences.

[38]  D. Alais,et al.  Orientation tuning of contrast masking caused by motion streaks. , 2010, Journal of vision.

[39]  Alexandre Pouget,et al.  A computational perspective on the neural basis of multisensory spatial representations , 2002, Nature Reviews Neuroscience.

[40]  Nancy Kanwisher,et al.  Cerebral Cortex doi:10.1093/cercor/bhr357 Higher Level Visual Cortex Represents Retinotopic, Not Spatiotopic, Object Location , 2011 .

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

[42]  Julie D. Golomb,et al.  The Native Coordinate System of Spatial Attention Is Retinotopic , 2008, The Journal of Neuroscience.

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

[44]  L. Maloney,et al.  Perceptual organization and neural computation. , 2008, Journal of vision.

[45]  Susana T. L. Chung,et al.  The dependence of crowding on flanker complexity and target-flanker similarity. , 2011, Journal of vision.

[46]  S. Hochstein,et al.  Learning Pop-out Detection: Specificities to Stimulus Characteristics , 1996, Vision Research.

[47]  Bruno B Averbeck,et al.  Representing spatial relationships in posterior parietal cortex: single neurons code object-referenced position. , 2007, Cerebral cortex.

[48]  D. Sagi Perceptual learning in Vision Research , 2011, Vision Research.

[49]  Xueting Li,et al.  The Role of Top-Down Task Context in Learning to Perceive Objects , 2010, The Journal of Neuroscience.

[50]  C. Genovese,et al.  Remapping in human visual cortex. , 2007, Journal of neurophysiology.

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

[52]  Dennis M. Levi,et al.  Decoupling location specificity from perceptual learning of orientation discrimination , 2010, Vision Research.

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

[54]  D. Burr,et al.  Spatiotopic selectivity of BOLD responses to visual motion in human area MT , 2007, Nature Neuroscience.

[55]  Simona Celebrini,et al.  Privileged Processing of the Straight-Ahead Direction in Primate Area V1 , 2010, Neuron.

[56]  Haluk Öğmen,et al.  Perceptual Learning in a Nonretinotopic Frame of Reference , 2010, Psychological science.

[57]  T. Poggio,et al.  Fast perceptual learning in hyperacuity , 1995, Vision Research.

[58]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[59]  David Melcher,et al.  Dynamic, object-based remapping of visual features in trans-saccadic perception. , 2008, Journal of vision.

[60]  G. Orban,et al.  The effect of practice on the oblique effect in line orientation judgments , 1985, Vision Research.

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

[62]  Bart Krekelberg,et al.  Summation of Visual Motion across Eye Movements Reflects a Nonspatial Decision Mechanism , 2010, The Journal of Neuroscience.

[63]  C. Genovese,et al.  Spatial Updating in Human Parietal Cortex , 2003, Neuron.

[64]  David C. Burr,et al.  Spatiotopic Coding of BOLD Signal in Human Visual Cortex Depends on Spatial Attention , 2011, PloS one.

[65]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[66]  David Melcher,et al.  Spatiotopic temporal integration of visual motion across saccadic eye movements , 2003, Nature Neuroscience.

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

[68]  C. Gilbert,et al.  Perceptual learning of spatial localization: specificity for orientation, position, and context. , 1997, Journal of neurophysiology.

[69]  Bruno B Averbeck,et al.  Neural Ensemble Decoding Reveals a Correlate of Viewer- to Object-Centered Spatial Transformation in Monkey Parietal Cortex , 2008, The Journal of Neuroscience.

[70]  H. Spekreijse,et al.  Correlates of transsaccadic integration in the primary visual cortex of the monkey. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[71]  T. Womelsdorf,et al.  Dynamic shifts of visual receptive fields in cortical area MT by spatial attention , 2006, Nature Neuroscience.

[72]  John M. Allman,et al.  The Effect of Gaze Angle and Fixation Distance on the Responses of Neurons in V1, V2, and V4 , 2002, Neuron.

[73]  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.

[74]  Peter König,et al.  Influence of disparity on fixation and saccades in free viewing of natural scenes. , 2009, Journal of vision.

[75]  C. Gilbert,et al.  Adult Visual Cortical Plasticity , 2012, Neuron.

[76]  S. Shipp The brain circuitry of attention , 2004, Trends in Cognitive Sciences.

[77]  C. Gilbert,et al.  Learning to Link Visual Contours , 2008, Neuron.

[78]  Patrick Cavanagh,et al.  The reference frame of the tilt aftereffect. , 2011, Journal of vision.

[79]  Ehud Zohary,et al.  Beyond retinotopic mapping: the spatial representation of objects in the human lateral occipital complex. , 2007, Cerebral cortex.