Spatiotopic Coding of BOLD Signal in Human Visual Cortex Depends on Spatial Attention

The neural substrate of the phenomenological experience of a stable visual world remains obscure. One possible mechanism would be to construct spatiotopic neural maps where the response is selective to the position of the stimulus in external space, rather than to retinal eccentricities, but evidence for these maps has been inconsistent. Here we show, with fMRI, that when human subjects perform concomitantly a demanding attentive task on stimuli displayed at the fovea, BOLD responses evoked by moving stimuli irrelevant to the task were mostly tuned in retinotopic coordinates. However, under more unconstrained conditions, where subjects could attend easily to the motion stimuli, BOLD responses were tuned not in retinal but in external coordinates (spatiotopic selectivity) in many visual areas, including MT, MST, LO and V6, agreeing with our previous fMRI study. These results indicate that spatial attention may play an important role in mediating spatiotopic selectivity.

[1]  M. Sereno,et al.  Retinotopy and Attention in Human Occipital, Temporal, Parietal, and Frontal Cortex , 2008 .

[2]  D. Heeger,et al.  Topographic maps of visual spatial attention in human parietal cortex. , 2005, Journal of neurophysiology.

[3]  Electrophysiological and behavioural evidence for the role of oculomotor proprioception on visual functions of the cat , 1984, Documenta Ophthalmologica.

[4]  Jacques Droulez,et al.  Self-motion and the perception of stationary objects , 2001, Nature.

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

[6]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[7]  J. Theeuwes,et al.  Gradual Remapping Results in Early Retinotopic and Late Spatiotopic Inhibition of Return , 2010, Psychological science.

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

[9]  C D Frith,et al.  Modulating irrelevant motion perception by varying attentional load in an unrelated task. , 1997, Science.

[10]  C. Colby,et al.  Trans-saccadic perception , 2008, Trends in Cognitive Sciences.

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

[12]  Dynamics of eye position signals in macaque dorsal areas explain peri-saccadic mislocalization , 2010 .

[13]  Ravi S. Menon,et al.  Representation of Head-Centric Flow in the Human Motion Complex , 2006, The Journal of Neuroscience.

[14]  P. Thier,et al.  Posterior Parietal Cortex Neurons Encode Target Motion in World-Centered Coordinates , 2004, Neuron.

[15]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

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

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

[18]  Yong Gu,et al.  Spatiotemporal properties of vestibular responses in area MSTd. , 2010, Journal of neurophysiology.

[19]  E. Zohary,et al.  Rapid Formation of Spatiotopic Representations As Revealed by Inhibition of Return , 2010, The Journal of Neuroscience.

[20]  Y. Cohen,et al.  Eye-centered, head-centered, and complex coding of visual and auditory targets in the intraparietal sulcus. , 2005, Journal of neurophysiology.

[21]  David Whitney,et al.  Attention Narrows Position Tuning of Population Responses in V1 , 2009, Current Biology.

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

[23]  Katherine M. Armstrong,et al.  Visuomotor Origins of Covert Spatial Attention , 2003, Neuron.

[24]  Charles J. Duffy,et al.  Cortical Neurons Encoding Path and Place: Where You Go Is Where You Are , 2002, Science.

[25]  Tutis Vilis,et al.  Eye position signals modulate early dorsal and ventral visual areas. , 2002, Cerebral cortex.

[26]  Bremmer,et al.  Eye position encoding in the macaque posterior parietal cortex , 1998, The European journal of neuroscience.

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

[28]  M. Sereno,et al.  A human parietal face area contains aligned head-centered visual and tactile maps , 2006, Nature Neuroscience.

[29]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

[30]  E. DeYoe,et al.  A physiological correlate of the 'spotlight' of visual attention , 1999, Nature Neuroscience.

[31]  S. Kastner,et al.  Topographic maps in human frontal and parietal cortex , 2009, Trends in Cognitive Sciences.

[32]  Markus Lappe,et al.  Visual selectivity for heading in monkey area MST , 2009, Experimental Brain Research.

[33]  C. Galletti,et al.  Human V6: The Medial Motion Area , 2009, Cerebral cortex.

[34]  D. Heeger,et al.  Spatial attention affects brain activity in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[36]  Kathleen A. Hansen,et al.  Topographic Organization in and near Human Visual Area V4 , 2007, The Journal of Neuroscience.

[37]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

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

[39]  Avishai Henik,et al.  Parietal Lobe Lesions Disrupt Saccadic Remapping of Inhibitory Location Tagging , 2004, Journal of Cognitive Neuroscience.

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

[41]  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.

[42]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI II. Analysis , 2001, NeuroImage.

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

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

[45]  A. Dale,et al.  The Retinotopy of Visual Spatial Attention , 1998, Neuron.

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

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

[48]  D. Heeger,et al.  Retinotopy and Functional Subdivision of Human Areas MT and MST , 2002, The Journal of Neuroscience.

[49]  S. Sterbing-D’Angelo,et al.  Behavioral/systems/cognitive Multisensory Space Representations in the Macaque Ventral Intraparietal Area , 2022 .

[50]  J. Bisley,et al.  Psychophysical evidence for spatiotopic processing in area MT in a short-term memory for motion task. , 2009, Journal of neurophysiology.

[51]  T. Pasternak,et al.  Area MT neurons respond to visual motion distant from their receptive fields. , 2005, Journal of neurophysiology.

[52]  M. Mesulam Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[53]  Abraham Z. Snyder,et al.  Transient BOLD responses at block transitions , 2005, NeuroImage.

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

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

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

[57]  Maria Concetta Morrone,et al.  Spatiotopic coding and remapping in humans , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[58]  D. Heeger,et al.  Two Retinotopic Visual Areas in Human Lateral Occipital Cortex , 2006, The Journal of Neuroscience.

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

[60]  David Melcher,et al.  The role of attention in central and peripheral motion integration , 2004, Vision Research.

[61]  P. Fox,et al.  Intersubject variability of functional areas in the human visual cortex , 1998, Human brain mapping.

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

[63]  D. Burr,et al.  A cortical area that responds specifically to optic flow, revealed by fMRI , 2000, Nature Neuroscience.

[64]  R. Andersen,et al.  The influence of the angle of gaze upon the excitability of the light- sensitive neurons of the posterior parietal cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[67]  Mark D'Esposito,et al.  Top-down flow of visual spatial attention signals from parietal to occipital cortex. , 2009, Journal of vision.

[68]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[69]  Yale E. Cohen,et al.  A common reference frame for movement plans in the posterior parietal cortex , 2002, Nature Reviews Neuroscience.