An fMRI study of visual hemifield integration and cerebral lateralization

&NA; The human brain integrates hemifield‐split visual information via interhemispheric transfer. The degree to which neural circuits involved in this process behave differently during word recognition as compared to object recognition is not known. Evidence from neuroimaging (fMRI) suggests that interhemispheric transfer during word viewing converges in the left hemisphere, in two distinct brain areas, an “occipital word form area” (OWFA) and a more anterior occipitotemporal “visual word form area” (VWFA). We used a novel fMRI half‐field repetition technique to test whether or not these areas also integrate nonverbal hemifield‐split string stimuli of similar visual complexity. We found that the fMRI responses of both the OWFA and VWFA while viewing nonverbal stimuli were strikingly different than those measured during word viewing, especially with respect to half‐stimulus changes restricted to a single hemifield. We conclude that normal reading relies on left‐lateralized neural mechanisms, which integrate hemifield‐split visual information for words but not for nonverbal stimuli. HighlightsResults are reported from an fMRI half‐field repetition paradigm.Left and right hemispheres show distinct patterns of repetition suppression.Half‐field suppression is different for words and non‐verbal stimuli.An occipital word form area (OWFA) underlies split‐word binding.

[1]  Marc Brysbaert,et al.  The importance of interhemispheric transfer for foveal vision: A factor that has been overlooked in theories of visual word recognition and object perception , 2004, Brain and Language.

[2]  D. Plaut,et al.  Distributed circuits, not circumscribed centers, mediate visual recognition , 2013, Trends in Cognitive Sciences.

[3]  Steven Z. Rapcsak,et al.  Efficient Visual Object and Word Recognition Relies on High Spatial Frequency Coding in the Left Posterior Fusiform Gyrus: Evidence from a Case-Series of Patients with Ventral Occipito-Temporal Cortex Damage , 2012, Cerebral cortex.

[4]  Tutis Vilis,et al.  Equal degrees of object selectivity for upper and lower visual field stimuli. , 2010, Journal of neurophysiology.

[5]  Marc Brysbaert,et al.  Split fovea theory and the role of the two cerebral hemispheres in reading: A review of the evidence , 2010, Neuropsychologia.

[6]  D M Levi,et al.  Perception of mirror symmetry reveals long‐range interactions between orientation‐selective cortical filters , 2000, Neuroreport.

[7]  Nava Rubin,et al.  Perceptual Completion across the Vertical Meridian and the Role of Early Visual Cortex , 2002, Neuron.

[8]  Karen F. LaRocque,et al.  Where is human V4? Predicting the location of hV4 and VO1 from cortical folding. , 2014, Cerebral cortex.

[9]  Laurie S. Glezer,et al.  Evidence for Highly Selective Neuronal Tuning to Whole Words in the “Visual Word Form Area” , 2009, Neuron.

[10]  G. Rhodes,et al.  The fusiform face area and occipital face area show sensitivity to spatial relations in faces , 2009, The European journal of neuroscience.

[11]  B. Wandell,et al.  Functional organization of human occipital-callosal fiber tracts. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Padraic Monaghan,et al.  Hemispheric dissociation and dyslexia in a computational model of reading , 2008, Brain and Language.

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

[14]  Matthias Niemeier,et al.  A contralateral preference in the lateral occipital area: sensory and attentional mechanisms. , 2004, Cerebral cortex.

[15]  Andrew W. Ellis,et al.  Interhemispheric cooperation and non-cooperation during word recognition: Evidence for callosal transfer dysfunction in dyslexic adults , 2007, Brain and Language.

[16]  S. Cool,et al.  Binocular depth perception and the corpus callosum , 1971 .

[17]  Brian A. Wandell,et al.  Position sensitivity in the visual word form area , 2012, Proceedings of the National Academy of Sciences.

[18]  S. Dehaene,et al.  Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area. , 2002, Brain : a journal of neurology.

[19]  Brian A. Wandell,et al.  Anatomy of the visual word form area: Adjacent cortical circuits and long-range white matter connections , 2013, Brain and Language.

[20]  Maximilian Riesenhuber,et al.  Adding Words to the Brain's Visual Dictionary: Novel Word Learning Selectively Sharpens Orthographic Representations in the VWFA , 2015, The Journal of Neuroscience.

[21]  Wolf Singer,et al.  Interhemispheric Connections Shape Subjective Experience of Bistable Motion , 2011, Current Biology.

[22]  Marlene Behrmann,et al.  The joint development of hemispheric lateralization for words and faces. , 2012, Journal of experimental psychology. General.

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

[24]  Nestor Matthews,et al.  Left visual field attentional advantage in judging simultaneity and temporal order. , 2015, Journal of vision.

[25]  Garrison W. Cottrell,et al.  Convergence of the Visual Field Split: Hemispheric Modeling of Face and Object Recognition , 2008, Journal of Cognitive Neuroscience.

[26]  Juha Silvanto,et al.  The Causal Role of the Occipital Face Area (OFA) and Lateral Occipital (LO) Cortex in Symmetry Perception , 2015, The Journal of Neuroscience.

[27]  R. Shillcock,et al.  Dyslexics' eye fixations may accommodate to hemispheric desynchronization , 2004, Neuroreport.

[28]  S. Petersen,et al.  The VWFA: it's not just for words anymore , 2014, Front. Hum. Neurosci..

[29]  R. Goebel BRAINVOYAGER: a program for analyzing and visualizing functional and structural magnetic resonance data sets , 1996, NeuroImage.

[30]  S. Trauzettel-Klosinski,et al.  Nasotemporal overlap of retinal ganglion cells in humans: a functional study. , 2003, Investigative ophthalmology & visual science.

[31]  Tutis Vilis,et al.  Visual Cortical Representation of Whole Words and Hemifield-split Word Parts , 2016, Journal of Cognitive Neuroscience.

[32]  S. Dehaene,et al.  Visual word recognition in the left and right hemispheres: anatomical and functional correlates of peripheral alexias. , 2003, Cerebral cortex.

[33]  S. Petersen,et al.  The left occipitotemporal cortex does not show preferential activity for words. , 2012, Cerebral cortex.

[34]  Walsh,et al.  Opinion - The nature of foveal representation , 2004 .

[35]  Cathy J. Price,et al.  Explaining Left Lateralization for Words in the Ventral Occipitotemporal Cortex , 2011, The Journal of Neuroscience.

[36]  K. Grill-Spector,et al.  Relating retinotopic and object-selective responses in human lateral occipital cortex. , 2008, Journal of neurophysiology.

[37]  G. Yovel,et al.  TMS Evidence for the Involvement of the Right Occipital Face Area in Early Face Processing , 2007, Current Biology.

[38]  Michal Lavidor,et al.  The nature of foveal representation , 2004, Nature Reviews Neuroscience.

[39]  Sheng He,et al.  Locating the cortical bottleneck for slow reading in peripheral vision. , 2015, Journal of vision.

[40]  D. Pitcher,et al.  The role of the occipital face area in the cortical face perception network , 2011, Experimental Brain Research.

[41]  Klaas E. Stephan,et al.  Mechanisms of hemispheric lateralization: Asymmetric interhemispheric recruitment in the face perception network , 2016, NeuroImage.

[42]  D. Plaut,et al.  The neural basis of visual word form processing: a multivariate investigation. , 2013, Cerebral cortex.

[43]  Samantha F. McCormick,et al.  Brain mechanisms of recovery from pure alexia: A single case study with multiple longitudinal scans , 2016, Neuropsychologia.

[44]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[45]  Giovanni Berlucchi,et al.  Visual interhemispheric communication and callosal connections of the occipital lobes , 2014, Cortex.

[46]  Randolph Blake,et al.  The Occipital Face Area Is Causally Involved in Facial Viewpoint Perception , 2015, The Journal of Neuroscience.

[47]  N. Kanwisher,et al.  A Preference for Contralateral Stimuli in Human Object- and Face-Selective Cortex , 2007, PloS one.

[48]  Régine Kolinsky,et al.  Illiterate to literate: behavioural and cerebral changes induced by reading acquisition , 2015, Nature Reviews Neuroscience.

[50]  Jia Liu,et al.  Perception of Face Parts and Face Configurations: An fMRI Study , 2010, Journal of Cognitive Neuroscience.

[51]  Stanislas Dehaene,et al.  Breaking the symmetry: Mirror discrimination for single letters but not for pictures in the Visual Word Form Area , 2011, NeuroImage.

[52]  G K Humphrey,et al.  Bilateral Symmetry Detection: Testing a ‘Callosal’ Hypothesis , 1996, Perception.

[53]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[54]  R. Rosenfeld Patients , 2012, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[55]  M. Sereno,et al.  Dissociation of Sensitivity to Spatial Frequency in Word and Face Preferential Areas of the Fusiform Gyrus , 2011, Cerebral cortex.

[56]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[57]  G. Orban,et al.  The Retinotopic Organization of the Human Middle Temporal Area MT/V5 and Its Cortical Neighbors , 2010, The Journal of Neuroscience.

[58]  Hidenao Fukuyama,et al.  Hemispheric asymmetry emerges at distinct parts of the occipitotemporal cortex for objects, logograms and phonograms: A functional MRI study , 2005, NeuroImage.

[59]  Marc Brysbaert,et al.  Foveal Word Reading Requires Interhemispheric Communication , 2007, Journal of Cognitive Neuroscience.

[60]  Matthew K. Leonard,et al.  Facial emotion recognition in agenesis of the corpus callosum , 2014, Journal of Neurodevelopmental Disorders.

[61]  D. Le Bihan,et al.  Visualizing the Neural Bases of a Disconnection Syndrome with Diffusion Tensor Imaging , 2002, Journal of Cognitive Neuroscience.

[62]  T. Vilis,et al.  Face Inversion Reduces the Persistence of Global Form and Its Neural Correlates , 2011, PLoS ONE.

[63]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[64]  S. Dehaene,et al.  How Learning to Read Changes the Cortical Networks for Vision and Language , 2010, Science.

[65]  F. Fabbro,et al.  Callosal Transfer in Different Subtypes of Developmental Dyslexia , 2001, Cortex.