Enhanced peripheral visual processing in congenitally deaf humans is supported by multiple brain regions, including primary auditory cortex

Brain reorganization associated with altered sensory experience clarifies the critical role of neuroplasticity in development. An example is enhanced peripheral visual processing associated with congenital deafness, but the neural systems supporting this have not been fully characterized. A gap in our understanding of deafness-enhanced peripheral vision is the contribution of primary auditory cortex. Previous studies of auditory cortex that use anatomical normalization across participants were limited by inter-subject variability of Heschl's gyrus. In addition to reorganized auditory cortex (cross-modal plasticity), a second gap in our understanding is the contribution of altered modality-specific cortices (visual intramodal plasticity in this case), as well as supramodal and multisensory cortices, especially when target detection is required across contrasts. Here we address these gaps by comparing fMRI signal change for peripheral vs. perifoveal visual stimulation (11–15° vs. 2–7°) in congenitally deaf and hearing participants in a blocked experimental design with two analytical approaches: a Heschl's gyrus region of interest analysis and a whole brain analysis. Our results using individually-defined primary auditory cortex (Heschl's gyrus) indicate that fMRI signal change for more peripheral stimuli was greater than perifoveal in deaf but not in hearing participants. Whole-brain analyses revealed differences between deaf and hearing participants for peripheral vs. perifoveal visual processing in extrastriate visual cortex including primary auditory cortex, MT+/V5, superior-temporal auditory, and multisensory and/or supramodal regions, such as posterior parietal cortex (PPC), frontal eye fields, anterior cingulate, and supplementary eye fields. Overall, these data demonstrate the contribution of neuroplasticity in multiple systems including primary auditory cortex, supramodal, and multisensory regions, to altered visual processing in congenitally deaf adults.

[1]  G. Essick,et al.  Tactile motion activates the human middle temporal/V5 (MT/V5) complex , 2002, The European journal of neuroscience.

[2]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[3]  Michael S. Beauchamp,et al.  A Parametric fMRI Study of Overt and Covert Shifts of Visuospatial Attention , 2001, NeuroImage.

[4]  Ione Fine,et al.  Visual stimuli activate auditory cortex in the deaf , 2001, Nature Neuroscience.

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

[6]  Helen J. Neville,et al.  Attention to central and peripheral visual space in a movement detection task: an event-related potential and behavioral study. I. Normal hearing adults , 1987, Brain Research.

[7]  A. Kral,et al.  Absence of cross-modal reorganization in the primary auditory cortex of congenitally deaf cats , 2003, Experimental Brain Research.

[8]  Ione Fine,et al.  Comparing the Effects of Auditory Deprivation and Sign Language within the Auditory and Visual Cortex , 2005, Journal of Cognitive Neuroscience.

[9]  Richard S. J. Frackowiak,et al.  Human Primary Auditory Cortex Follows the Shape of Heschl's Gyrus , 2011, The Journal of Neuroscience.

[10]  Karen R. Dobkins,et al.  The Effects of Spatial Attention on Motion Processing in Deaf Signers, Hearing Signers, and Hearing Nonsigners , 2002, Brain and Cognition.

[11]  Hanna Damasio,et al.  A morphometric analysis of auditory brain regions in congenitally deaf adults , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  S. Levänen,et al.  Vibration-induced auditory-cortex activation in a congenitally deaf adult , 1998, Current Biology.

[13]  P. Matthews,et al.  Independent anatomical and functional measures of the V1/V2 boundary in human visual cortex. , 2005, Journal of vision.

[14]  Karl J. Friston,et al.  The functional anatomy of attention to visual motion. A functional MRI study. , 1998, Brain : a journal of neurology.

[15]  Xavier Golay,et al.  Retinotopic mapping in the human visual cortex using vascular space occupancy-dependent functional magnetic resonance imaging , 2005, Neuroreport.

[16]  F. Lepore,et al.  Reorganization of the auditory, visual and multimodal areas in early deaf individuals , 2013, Neuroscience.

[17]  Matthew W. G. Dye,et al.  Do deaf individuals see better? , 2006, Trends in Cognitive Sciences.

[18]  D. Shibata,et al.  Differences in brain structure in deaf persons on MR imaging studied with voxel-based morphometry. , 2007, AJNR. American journal of neuroradiology.

[19]  H. Neville,et al.  Altered Cross-Modal Processing in the Primary Auditory Cortex of Congenitally Deaf Adults: A Visual-Somatosensory fMRI Study with a Double-Flash Illusion , 2012, The Journal of Neuroscience.

[20]  M. Meredith,et al.  Multisensory dysfunction accompanies crossmodal plasticity following adult hearing impairment , 2012, Neuroscience.

[21]  M. Crawford,et al.  The sensitive period. , 1979, Transactions of the ophthalmological societies of the United Kingdom.

[22]  Helen J. Neville,et al.  Attention to central and peripheral visual space in a movement detection task: an event-related potential and behavioral study. II. Congenitally deaf adults , 1987, Brain Research.

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

[24]  M. Giard,et al.  Changes in Early Cortical Visual Processing Predict Enhanced Reactivity in Deaf Individuals , 2011, PloS one.

[25]  A. Dale,et al.  Functional Parcellation of Attentional Control Regions of the Brain , 2004, Journal of Cognitive Neuroscience.

[26]  Ikuko Mukai,et al.  Activations in Visual and Attention-Related Areas Predict and Correlate with the Degree of Perceptual Learning , 2007, The Journal of Neuroscience.

[27]  J P Rauschecker,et al.  Hemispheric specialization for English and ASL: left invariance‐right variability , 1998, Neuroreport.

[28]  M. Meredith,et al.  Adult deafness induces somatosensory conversion of ferret auditory cortex , 2009, Proceedings of the National Academy of Sciences.

[29]  T. Hackett.  Information flow in the auditory cortical network , 2011, Hearing Research.

[30]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[31]  B. A. Sabel,et al.  Altered White Matter Integrity in Adolescents with Prelingual Deafness: A High-Resolution Tract-Based Spatial Statistics Imaging Study , 2013, American Journal of Neuroradiology.

[32]  Wing Hong Lore,et al.  Central and peripheral visual processing in hearing and nonhearing individuals , 1991 .

[33]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[34]  Witaya Sungkarat,et al.  Vibrotactile activation of the auditory cortices in deaf versus hearing adults , 2007, Neuroreport.

[35]  Helen J. Neville,et al.  Neuroplasticity as a Double-edged Sword: Deaf Enhancements and Dyslexic Deficits in Motion Processing , 2006, Journal of Cognitive Neuroscience.

[36]  Aaron J. Newman,et al.  A critical period for right hemisphere recruitment in American Sign Language processing , 2002, Nature Neuroscience.

[37]  Richard S. J. Frackowiak,et al.  Functional localization of the system for visuospatial attention using positron emission tomography. , 1997, Brain : a journal of neurology.

[38]  D Bavelier,et al.  Cerebral organization for language in deaf and hearing subjects: biological constraints and effects of experience. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[40]  C. Hutton,et al.  Visual Attention to the Periphery Is Enhanced in Congenitally Deaf Individuals , 2000, The Journal of Neuroscience.

[41]  M. Sereno,et al.  Neural organization for recognition of grammatical and emotional facial expressions in deaf ASL signers and hearing nonsigners. , 2005, Brain research. Cognitive brain research.

[42]  Yong He,et al.  Sensitive period for white‐matter connectivity of superior temporal cortex in deaf people , 2012, Human brain mapping.

[43]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[44]  Marta Kutas,et al.  Altered visual-evoked potentials in congenitally deaf adults , 1983, Brain Research.

[45]  Kenith V. Sobel,et al.  Neural Synergy Between Kinetic Vision and Touch , 2004, Psychological science.

[46]  D. Bavelier,et al.  Cross-modal plasticity: where and how? , 2002, Nature Reviews Neuroscience.

[47]  R. Deichmann,et al.  Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. , 2008, Cerebral cortex.

[48]  P. Morosan,et al.  Human Primary Auditory Cortex: Cytoarchitectonic Subdivisions and Mapping into a Spatial Reference System , 2001, NeuroImage.

[49]  S. Lomber,et al.  Somatosensory and visual crossmodal plasticity in the anterior auditory field of early-deaf cats , 2011, Hearing Research.

[50]  Martin Meyer,et al.  Neuroplasticity of sign language: implications from structural and functional brain imaging. , 2007, Restorative neurology and neuroscience.

[51]  A. Dale,et al.  Functional analysis of primary visual cortex (V1) in humans. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Karen R. Dobkins,et al.  Visual Field Asymmetries for Motion Processing in Deaf and Hearing Signers , 2002, Brain and Cognition.

[53]  B. Argall,et al.  Unraveling multisensory integration: patchy organization within human STS multisensory cortex , 2004, Nature Neuroscience.

[54]  H. Neville,et al.  Attention to central and peripheral visual space in a movement detection task. III. Separate effects of auditory deprivation and acquisition of a visual language , 1987, Brain Research.

[55]  Andrew B. Leber,et al.  Coordination of Voluntary and Stimulus-Driven Attentional Control in Human Cortex , 2005, Psychological science.

[56]  N. Fox,et al.  VI. Sensitive periods , 2011 .

[57]  O. Andreassen,et al.  Mice Deficient in Cellular Glutathione Peroxidase Show Increased Vulnerability to Malonate, 3-Nitropropionic Acid, and 1-Methyl-4-Phenyl-1,2,5,6-Tetrahydropyridine , 2000, The Journal of Neuroscience.

[58]  S. Lomber,et al.  Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf , 2010, Nature Neuroscience.

[59]  Leslie P. Keniston,et al.  Auditory influences on non-auditory cortices , 2009, Hearing Research.

[60]  Joseph A Maldjian,et al.  Cross‐modal sensory processing in the anterior cingulate and medial prefrontal cortices , 2003, Human brain mapping.

[61]  C. Schroeder,et al.  Neuronal mechanisms, response dynamics and perceptual functions of multisensory interactions in auditory cortex , 2009, Hearing Research.

[62]  Hae-Jeong Park,et al.  Alterations of white matter diffusion anisotropy in early deafness , 2009, Neuroreport.

[63]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[64]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

[65]  Craig J. Brozinsky,et al.  Impact of Early Deafness and Early Exposure to Sign Language on the Cerebral Organization for Motion Processing , 2001, The Journal of Neuroscience.

[66]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[67]  John J. Foxe,et al.  Multisensory contributions to low-level, ‘unisensory’ processing , 2005, Current Opinion in Neurobiology.

[68]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.