Time-course of Posterior Parietal and Occipital Cortex Contribution to Sound Localization

It has been suggested that both the posterior parietal cortex (PPC) and the extrastriate occipital cortex (OC) participate in the spatial processing of sounds. However, the precise time-course of their contribution remains unknown, which is of particular interest, considering that it could give new insights into the mechanisms underlying auditory space perception. To address this issue, we have used event-related transcranial magnetic stimulation (TMS) to induce virtual lesions of either the right PPC or right OC at different delays in subjects performing a sound lateralization task. Our results confirmed that these two areas participate in the spatial processing of sounds. More precisely, we found that TMS applied over the right OC 50 msec after the stimulus onset significantly impaired the localization of sounds presented either to the right or to the left side. Moreover, right PPC virtual lesions induced 100 and 150 msec after sound presentation led to a rightward bias for stimuli delivered on the center and on the left side, reproducing transiently the deficits commonly observed in hemineglect patients. The finding that the right OC is involved in sound processing before the right PPC suggests that the OC exerts a feedforward influence on the PPC during auditory spatial processing.

[1]  Roger Strong,et al.  Selective up‐regulation of IκB‐α in ischemic penumbra following focal cerebral ischemia , 2000 .

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

[3]  J. Duhamel,et al.  Audio-Spatial Deficits in Humans: Differential Effects Associated with Left Versus Right Hemisphere Parietal Damage , 1989, Cortex.

[4]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

[5]  J. Rauschecker,et al.  A PET study of human auditory spatial processing , 1999, Neuroscience Letters.

[6]  J. Blauert.  Spatial Hearing: The Psychophysics of Human Sound Localization , 1983 .

[7]  Richard S. J. Frackowiak,et al.  Right parietal cortex is involved in the perception of sound movement in humans , 1998, Nature Neuroscience.

[8]  K. Palomäki,et al.  Spatial processing in human auditory cortex: the effects of 3D, ITD, and ILD stimulation techniques. , 2005, Brain research. Cognitive brain research.

[9]  R. Andersen,et al.  Eye-centered, head-centered, and intermediate coding of remembered sound locations in area LIP. , 1996, Journal of neurophysiology.

[10]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[11]  M. Davare,et al.  Reorganisation of the Right Occipito-Parietal Stream for Auditory Spatial Processing in Early Blind Humans. A Transcranial Magnetic Stimulation Study , 2009, Brain Topography.

[12]  E. Wassermann,et al.  A safety screening questionnaire for transcranial magnetic stimulation , 2001, Clinical Neurophysiology.

[13]  C. Galletti,et al.  Eye Position Influence on the Parieto‐occipital Area PO (V6) of the Macaque Monkey , 1995, The European journal of neuroscience.

[14]  M. Davare,et al.  Temporal Dissociation between Hand Shaping and Grip Force Scaling in the Anterior Intraparietal Area , 2007, The Journal of Neuroscience.

[15]  Michael Andres,et al.  Double dissociation between motor and visual imagery in the posterior parietal cortex. , 2009, Cerebral cortex.

[16]  Jon Driver,et al.  Auditory and multisensory aspects of visuospatial neglect , 2003, Trends in Cognitive Sciences.

[17]  Henry Kennedy,et al.  Long-distance feedback projections to area V1: Implications for multisensory integration, spatial awareness, and visual consciousness , 2004, Cognitive, affective & behavioral neuroscience.

[18]  Paavo Alku,et al.  Sound localization in the human brain: neuromagnetic observations , 2000, Neuroreport.

[19]  H. H. Chung,et al.  Dynamic representation of eye position in the parieto-occipital sulcus. , 1999, Journal of neurophysiology.

[20]  E. Macaluso,et al.  Multisensory spatial interactions: a window onto functional integration in the human brain , 2005, Trends in Neurosciences.

[21]  Rainer Goebel,et al.  Brain Network Dynamics Underlying Visuospatial Judgment: An fMRI Connectivity Study , 2010, Journal of Cognitive Neuroscience.

[22]  Alan Cowey,et al.  Spatial neglect in near and far space investigated by repetitive transcranial magnetic stimulation. , 2002, Brain : a journal of neurology.

[23]  J. Thiran,et al.  Distinct Pathways Involved in Sound Recognition and Localization: A Human fMRI Study , 2000, NeuroImage.

[24]  Jörg Lewald,et al.  Distortion of auditory space in hemianopia , 2009, The European journal of neuroscience.

[25]  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.

[26]  C. Veraart,et al.  Functional Cerebral Reorganization for Auditory Spatial Processing and Auditory Substitution of Vision in Early Blind Subjects , 2006 .

[27]  E. Bisiach,et al.  Disorders of perceived auditory lateralization after lesions of the right hemisphere. , 1984, Brain : a journal of neurology.

[28]  T. Griffiths,et al.  Distinct Mechanisms for Processing Spatial Sequences and Pitch Sequences in the Human Auditory Brain , 2003, The Journal of Neuroscience.

[29]  Anne Bol,et al.  Cross-modal activation of visual cortex during depth perception using auditory substitution of vision , 2005, NeuroImage.

[30]  Jon Driver,et al.  Auditory Deficits in Visuospatial Neglect Patients , 2004, Cortex.

[31]  Lucas Spierer,et al.  Auditory spatio-temporal brain dynamics and their consequences for multisensory interactions in humans , 2009, Hearing Research.

[32]  I. Meister,et al.  Involvement of the Superior Temporal Cortex and the Occipital Cortex in Spatial Hearing: Evidence from Repetitive Transcranial Magnetic Stimulation , 2004, Journal of Cognitive Neuroscience.

[33]  Á. Pascual-Leone,et al.  The metamodal organization of the brain. , 2001, Progress in brain research.

[34]  Paavo Alku,et al.  Neuromagnetic recordings reveal the temporal dynamics of auditory spatial processing in the human cortex , 2006, Neuroscience Letters.

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

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

[37]  Benoit M. Macq,et al.  Registration and real-time visualization of transcranial magnetic stimulation with 3-D MR images , 2004, IEEE Transactions on Biomedical Engineering.

[38]  J Driver,et al.  Crossmodal Spatial Influences of Touch on Extrastriate Visual Areas Take Current Gaze Direction into Account , 2002, Neuron.

[39]  A. Pouget,et al.  Reference frames for representing visual and tactile locations in parietal cortex , 2005, Nature Neuroscience.

[40]  Francesco Pavani,et al.  Poor hand-pointing to sounds in right brain-damaged patients: Not just a problem of spatial-hearing , 2005, Brain and Cognition.

[41]  FRANK MORRELL,et al.  Visual System's View of Acoustic Space , 1972, Nature.

[42]  J. Rauschecker,et al.  Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans , 1999, Nature Neuroscience.

[43]  T. Sejnowski,et al.  Early Cross-Modal Interactions in Auditory and Visual Cortex Underlie a Sound-Induced Visual Illusion , 2007, The Journal of Neuroscience.

[44]  M Lotze,et al.  Comparison of representational maps using functional magnetic resonance imaging and transcranial magnetic stimulation , 2003, Clinical Neurophysiology.

[45]  John J. Foxe,et al.  Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. , 2002, Brain research. Cognitive brain research.

[46]  Thomas F Münte,et al.  Transcranial magnetic stimulation to the parietal lobes reduces detection of contralateral somatosensory stimuli , 2004, Acta neurologica Scandinavica.

[47]  Kathleen S Rockland,et al.  Multisensory convergence in calcarine visual areas in macaque monkey. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[49]  Filippo Brighina,et al.  Contralateral neglect induced by right posterior parietal rTMS in healthy subjects , 2000, Neuroreport.

[50]  H Ogata,et al.  Sound lateralisation in patients with left or right cerebral hemispheric lesions: relation with unilateral visuospatial neglect , 1999, Journal of neurology, neurosurgery, and psychiatry.

[51]  M. Davare,et al.  Behavioral / Systems / Cognitive Dissociating the Role of Ventral and Dorsal Premotor Cortex in Precision Grasping , 2018 .

[52]  A. Ghazanfar,et al.  Is neocortex essentially multisensory? , 2006, Trends in Cognitive Sciences.

[53]  M. Giard,et al.  Auditory-Visual Integration during Multimodal Object Recognition in Humans: A Behavioral and Electrophysiological Study , 1999, Journal of Cognitive Neuroscience.

[54]  Jörg Lewald,et al.  Shift in sound localization induced by rTMS of the posterior parietal lobe , 2004, Neuropsychologia.

[55]  John J. Foxe,et al.  The case for feedforward multisensory convergence during early cortical processing , 2005, Neuroreport.

[56]  W. Ehrenstein,et al.  The effect of eye position on auditory lateralization , 2004, Experimental Brain Research.

[57]  J Driver,et al.  Influence of gaze direction on crossmodal modulation of visual ERPS by endogenous tactile spatial attention. , 2005, Brain research. Cognitive brain research.

[58]  Scott T. Grafton,et al.  Feeling with the mind's eye , 1997, Neuroreport.

[59]  J. Rauschecker,et al.  Mechanisms and streams for processing of "what" and "where" in auditory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[60]  R. Zatorre,et al.  Where is 'where' in the human auditory cortex? , 2002, Nature Neuroscience.

[61]  Jörg Lewald,et al.  The effect of gaze eccentricity on perceived sound direction and its relation to visual localization , 1998, Hearing Research.

[62]  C. Svarer,et al.  Parieto-occipital cortex activation during self-generated eye movements in the dark. , 1998, Brain : a journal of neurology.

[63]  H. Kennedy,et al.  Anatomical Evidence of Multimodal Integration in Primate Striate Cortex , 2002, The Journal of Neuroscience.

[64]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.

[65]  C. R. Michael,et al.  Integration of auditory information in the cat's visual cortex. , 1973, Vision research.

[66]  Gregor Thut,et al.  Dorsal posterior parietal rTMS affects voluntary orienting of visuospatial attention. , 2005, Cerebral cortex.

[67]  R. Töpper,et al.  Role of the Posterior Parietal Cortex in Spatial Hearing , 2002, The Journal of Neuroscience.

[68]  M. Lassonde,et al.  Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects , 2008, Experimental Brain Research.

[69]  A. Vanlierde,et al.  Specific activation of the V5 brain area by auditory motion processing: an fMRI study. , 2005, Brain research. Cognitive brain research.

[70]  Michael Erb,et al.  Is there a role of visual cortex in spatial hearing? , 2004, The European journal of neuroscience.