Retinotopic Mapping of Categorical and Coordinate Spatial Relation Processing in Early Visual Cortex

Spatial relations are commonly divided in two global classes. Categorical relations concern abstract relations which define areas of spatial equivalence, whereas coordinate relations are metric and concern exact distances. Categorical and coordinate relation processing are thought to rely on at least partially separate neurocognitive mechanisms, as reflected by differential lateralization patterns, in particular in the parietal cortex. In this study we address this textbook principle from a new angle. We studied retinotopic activation in early visual cortex, as a reflection of attentional distribution, in a spatial working memory task with either a categorical or a coordinate instruction. Participants were asked to memorize a dot position, with regard to a central cross, and to indicate whether a subsequent dot position matched the first dot position, either categorically (opposite quadrant of the cross) or coordinately (same distance to the centre of the cross). BOLD responses across the retinotopic maps of V1, V2, and V3 indicate that the spatial distribution of cortical activity was different for categorical and coordinate instructions throughout the retention interval; a more local focus was found during categorical processing, whereas focus was more global for coordinate processing. This effect was strongest for V3, approached significance in V2 and was absent in V1. Furthermore, during stimulus presentation the two instructions led to different levels of activation in V3 during stimulus encoding; a stronger increase in activity was found for categorical processing. Together this is the first demonstration that instructions for specific types of spatial relations may yield distinct attentional patterns which are already reflected in activity early in the visual cortex.

[1]  J. Hart,et al.  Hemispheric Asymmetry in Categorical Versus Coordinate Visuospatial Processing Revealed by Temporary Cortical Deactivation , 2001, Journal of Cognitive Neuroscience.

[2]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[3]  M Corbetta,et al.  Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[4]  David J Heeger,et al.  Neural correlates of sustained spatial attention in human early visual cortex. , 2007, Journal of neurophysiology.

[5]  M. Conson,et al.  Categorical and coordinate spatial processing in the imagery domain investigated by rTMS , 2006, Neuropsychologia.

[6]  A. Postma,et al.  The time course of hemispheric differences in categorical and coordinate spatial processing , 2007, Neuropsychologia.

[7]  N. Ramsey,et al.  Phase Navigator Correction in 3D fMRI Improves Detection of Brain Activation: Quantitative Assessment with a Graded Motor Activation Procedure , 1998, NeuroImage.

[8]  M. Lamb,et al.  The Two Sides of Perception , 1998, Trends in Cognitive Sciences.

[9]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[10]  S. Kosslyn Seeing and imagining in the cerebral hemispheres: a computational approach. , 1987, Psychological review.

[11]  R. Parasuraman The attentive brain , 1998 .

[12]  S. Kosslyn,et al.  Varying the scope of attention alters the encoding of categorical and coordinate spatial relations , 2010, Neuropsychologia.

[13]  S. Kosslyn,et al.  Categorical versus coordinate spatial relations: computational analyses and computer simulations. , 1992, Journal of experimental psychology. Human perception and performance.

[14]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[15]  G. Borst,et al.  Individual differences in spatial relation processing: Effects of strategy, ability, and gender , 2011, Brain and Cognition.

[16]  Albert Postma,et al.  Categorical and coordinate spatial relations in working memory: An fMRI study , 2009, Brain Research.

[17]  Bruno Laeng,et al.  Exogenous attention differentially modulates the processing of categorical and coordinate spatial relations. , 2010, Acta psychologica.

[18]  Albert Postma,et al.  Lateralization of spatial categories: A comparison of verbal and visuospatial categorical relations , 2010, Memory & cognition.

[19]  J. Jonides,et al.  Rehearsal in spatial working memory. , 1998, Journal of experimental psychology. Human perception and performance.

[20]  R. Desimone Visual attention mediated by biased competition in extrastriate visual cortex. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[21]  M H Van Kleeck,et al.  Hemispheric differences in global versus local processing of hierarchical visual stimuli by normal subjects: new data and a meta-analysis of previous studies. , 1989, Neuropsychologia.

[22]  Kara D. Federmeier,et al.  Categorical and Metric Spatial Processes Distinguished by Task Demands and Practice , 1999, Journal of Cognitive Neuroscience.

[23]  Bruno Laeng,et al.  Cerebral lateralization for the processing of spatial coordinates and categories in left- and right-handers , 1995, Neuropsychologia.

[24]  Y. Burnod,et al.  Is there continuity between categorical and coordinate spatial relations coding? Evidence from a grid/no-grid working memory paradigm , 2008, Neuropsychologia.

[25]  A. T. Smith,et al.  Estimating receptive field size from fMRI data in human striate and extrastriate visual cortex. , 2001, Cerebral cortex.

[26]  A. Postma,et al.  On the hemispheric specialization for categorical and coordinate spatial relations: a review of the current evidence , 2003, Neuropsychologia.

[27]  Bruno Laeng,et al.  Processing Spatial Relations With Different Apertures of Attention , 2011, Cogn. Sci..

[28]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[29]  Jan Theeuwes,et al.  Spatial working memory effects in early visual cortex , 2010, Brain and Cognition.

[30]  J Jonides,et al.  Human Rehearsal Processes and the Frontal Lobes: PET Evidence , 1995, Annals of the New York Academy of Sciences.

[31]  J. Hellige,et al.  Categorization versus distance: Hemispheric differences for processing spatial information , 1989, Memory & cognition.

[32]  R. Turner,et al.  Characterizing Evoked Hemodynamics with fMRI , 1995, NeuroImage.

[33]  D. Weinberger,et al.  Three-dimensional functional magnetic resonance imaging of human brain on a clinical 1.5-T scanner. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[35]  Robert A. Jacobs,et al.  Encoding Shape and Spatial Relations: The Role of Receptive Field Size in Coordinating Complementary Representations , 1994, Cogn. Sci..

[36]  C. B. Cave,et al.  Evidence for two types of spatial representations: hemispheric specialization for categorical and coordinate relations. , 1989, Journal of experimental psychology. Human perception and performance.

[37]  Keith J. Holyoak,et al.  Structure and Functions of the Human Prefrontal Cortex , 1996 .

[38]  R. Bruyer,et al.  Dissociation between Categorical and Coordinate Spatial Computations: Modulation by Cerebral Hemispheres, Task Properties, Mode of Response, and Age , 1997, Brain and Cognition.

[39]  C. Segebarth,et al.  Categorical and coordinate spatial relations: fMRI evidence for hemispheric specialization. , 1999, Neuroreport.