Hemispheric competence for auditory spatial representation.

Sound localization relies on the analysis of interaural time and intensity differences, as well as attenuation patterns by the outer ear. We investigated the relative contributions of interaural time and intensity difference cues to sound localization by testing 60 healthy subjects: 25 with focal left and 25 with focal right hemispheric brain damage. Group and single-case behavioural analyses, as well as anatomo-clinical correlations, confirmed that deficits were more frequent and much more severe after right than left hemispheric lesions and for the processing of interaural time than intensity difference cues. For spatial processing based on interaural time difference cues, different error types were evident in the individual data. Deficits in discriminating between neighbouring positions occurred in both hemispaces after focal right hemispheric brain damage, but were restricted to the contralesional hemispace after focal left hemispheric brain damage. Alloacusis (perceptual shifts across the midline) occurred only after focal right hemispheric brain damage and was associated with minor or severe deficits in position discrimination. During spatial processing based on interaural intensity cues, deficits were less severe in the right hemispheric brain damage than left hemispheric brain damage group and no alloacusis occurred. These results, matched to anatomical data, suggest the existence of a binaural sound localization system predominantly based on interaural time difference cues and primarily supported by the right hemisphere. More generally, our data suggest that two distinct mechanisms contribute to: (i) the precise computation of spatial coordinates allowing spatial comparison within the contralateral hemispace for the left hemisphere and the whole space for the right hemisphere; and (ii) the building up of global auditory spatial representations in right temporo-parietal cortices.

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

[2]  Claude Alain,et al.  Assessing the auditory dual-pathway model in humans , 2004, NeuroImage.

[3]  J. Kaiser,et al.  Location changes enhance hemispheric asymmetry of magnetic fields evoked by lateralized sounds in humans , 2001, Neuroscience Letters.

[4]  H. Karnath,et al.  Spatial orientation and the representation of space with parietal lobe lesions. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[5]  Jean-Philippe Thiran,et al.  What and Where in human audition: selective deficits following focal hemispheric lesions , 2002, Experimental Brain Research.

[6]  Chris Rorden,et al.  Spatial Normalization of Brain Images with Focal Lesions Using Cost Function Masking , 2001, NeuroImage.

[7]  Christoph M. Michel,et al.  Segregated Processing of Auditory Motion and Auditory Location: An ERP Mapping Study , 2002, NeuroImage.

[8]  Robert J. Zatorre,et al.  Spatial Localization after Excision of Human Auditory Cortex , 2001, The Journal of Neuroscience.

[9]  J. Rauschecker Parallel Processing in the Auditory Cortex of Primates , 1998, Audiology and Neurotology.

[10]  Raphaël V. Meylan,et al.  The spatio-temporal brain dynamics of processing and integrating sound localization cues in humans , 2006, Brain Research.

[11]  John C. Middlebrooks,et al.  Auditory space processing: here, there or everywhere? , 2002, Nature Neuroscience.

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

[13]  Lateralization and binaural discrimination of patients with pontine lesions. , 1998, The Journal of the Acoustical Society of America.

[14]  M Florentine,et al.  Critical band in auditory lateralization. , 1976, Sensory processes.

[15]  R. Levine,et al.  Effects of multiple sclerosis brainstem lesions on sound lateralization and brainstem auditory evoked potentials , 1993, Hearing Research.

[16]  L P SANCHEZ-LONGO,et al.  Clinical Significance of Impairment of Sound Localization , 1958, Neurology.

[17]  Christoph M. Michel,et al.  Cortical Motion Deafness , 2004, Neuron.

[18]  R Meuli,et al.  Two types of auditory neglect. , 2001, Brain : a journal of neurology.

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

[20]  Chris Rorden,et al.  The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. , 2004, Cerebral cortex.

[21]  E. Bisiach,et al.  Perceptual and premotor components of unilateral auditory neglect , 1996, Journal of the International Neuropsychological Society.

[22]  E. Yund,et al.  Central auditory processing III. The “cocktail party” effect and anterior temporal lobectomy , 1983, Brain and Language.

[23]  A. Rees,et al.  Evidence for a sound movement area in the human cerebral cortex , 1996, Nature.

[24]  J. A. Altman,et al.  Effects of unilateral disorder of the brain hemisphere function in man on directional hearing , 1979, Neuropsychologia.

[25]  N. Soroker,et al.  Auditory inattention in right-hemisphere-damaged patients with and without visual neglect , 1997, Neuropsychologia.

[26]  Lucas Spierer,et al.  Learning-Induced Plasticity in Auditory Spatial Representations Revealed by Electrical Neuroimaging , 2007, The Journal of Neuroscience.

[27]  Volker Hömberg,et al.  Sound localization in egocentric space following hemispheric lesions , 1996, Neuropsychologia.

[28]  M. Mishkin,et al.  Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex , 1999, Nature Neuroscience.

[29]  G. Green,et al.  A distinct low‐level mechanism for interaural timing analysis in human hearing , 1998, Neuroreport.

[30]  Natasa Kovacevic,et al.  Spatiotemporal analysis of auditory "what" and "where" working memory. , 2009, Cerebral cortex.

[31]  C. Grady,et al.  “What” and “where” in the human auditory system , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Duhamel,et al.  Multisensory Integration in the Ventral Intraparietal Area of the Macaque Monkey , 2007, The Journal of Neuroscience.

[33]  F. Dick,et al.  Voxel-based lesion–symptom mapping , 2003, Nature Neuroscience.

[34]  L. Rayleigh,et al.  XII. On our perception of sound direction , 1907 .

[35]  E. Walsh,et al.  An investigation of sound localization in patients with neurological abnormalities. , 1957, Brain : a journal of neurology.

[36]  John F. Brugge,et al.  The Structure of Spatial Receptive Fields of Neurons in Primary Auditory Cortex of the Cat , 1996, The Journal of Neuroscience.

[37]  K. Kaga,et al.  Sound lateralization in patients with lesions including the auditory cortex: comparison of interaural time difference (ITD) discrimination and interaural intensity difference (IID) discrimination , 1996, Hearing Research.

[38]  Lucas Spierer,et al.  The path to success in auditory spatial discrimination: Electrical neuroimaging responses within the supratemporal plane predict performance outcome , 2008, NeuroImage.

[39]  E. Bisiach,et al.  Spatial hemineglect in back space. , 1995, Brain : a journal of neurology.

[40]  K. Heilman,et al.  Mechanisms underlying hemispatial neglect , 1979, Annals of neurology.

[41]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[42]  Ivan Toni,et al.  Eye position tunes the contribution of allocentric and egocentric information to target localization in human goal-directed arm movements , 1997, Neuroscience Letters.

[43]  B. Shinn-Cunningham,et al.  Task-modulated “what” and “where” pathways in human auditory cortex , 2006, Proceedings of the National Academy of Sciences.

[44]  K. H. Pribram,et al.  Auditory spatial deficits in the personal and extrapersonal frames of reference due to cortical lesions , 1981, Neuropsychologia.

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

[46]  C Witton,et al.  Spatial and temporal auditory processing deficits following right hemisphere infarction. A psychophysical study. , 1997, Brain : a journal of neurology.

[47]  Stephanie Clarke,et al.  Automatic and intrinsic auditory "what" and "where" processing in humans revealed by electrical neuroimaging. , 2006, Cerebral cortex.

[48]  J. C. Middlebrooks,et al.  Coding of Sound-Source Location by Ensembles of Cortical Neurons , 2000, The Journal of Neuroscience.

[49]  Ewan A. Macpherson,et al.  Spatial sensitivity of neurons in the anterior, posterior, and primary fields of cat auditory cortex , 2008, Hearing Research.

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

[51]  M. Schönwiesner,et al.  Representation of interaural temporal information from left and right auditory space in the human planum temporale and inferior parietal lobe. , 2005, Cerebral cortex.

[52]  Jon Driver,et al.  Selective deficit of auditory localisation in patients with visuospatial neglect , 2002, Neuropsychologia.

[53]  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.

[54]  J. Kaas,et al.  Auditory processing in primate cerebral cortex , 1999, Current Opinion in Neurobiology.

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

[56]  E. Schröger,et al.  Interaural time and level differences: integrated or separated processing? , 1996, Hearing research.

[57]  Micah M. Murray,et al.  Rapid Brain Discrimination of Sounds of Objects , 2006, The Journal of Neuroscience.

[58]  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.

[59]  J. Winn,et al.  Brain , 1878, The Lancet.

[60]  A. Halliday,et al.  Scalp potentials following sudden coherence and discoherence of binaural noise and change in the inter-aural time difference: a specific binaural evoked potential or a "mismatch" response? , 1991, Electroencephalography and clinical neurophysiology.

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

[62]  R. Levine,et al.  Effects of localized pontine lesions on auditory brain-stem evoked potentials and binaural processing in humans. , 1998, Electroencephalography and clinical neurophysiology.

[63]  Lucas Spierer,et al.  Plasticity in representations of environmental sounds revealed by electrical neuroimaging , 2008, NeuroImage.

[64]  K. Reinikainen,et al.  Mismatch negativity to change in spatial location of an auditory stimulus. , 1989, Electroencephalography and clinical neurophysiology.

[65]  Robert A. A. Campbell,et al.  Physiological and behavioral studies of spatial coding in the auditory cortex , 2007, Hearing Research.

[66]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

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

[68]  R. Meuli,et al.  Auditory agnosia and auditory spatial deficits following left hemispheric lesions: evidence for distinct processing pathways , 2000, Neuropsychologia.

[69]  R. Levine,et al.  Brainstem lesions and click lateralization in patients with multiple sclerosis , 1995, Hearing Research.

[70]  J. Villemure,et al.  Sound localization in hemispherectomized patients , 1994, Neuropsychologia.

[71]  Lucas Spierer,et al.  Right hemispheric dominance for echo suppression , 2009, Neuropsychologia.

[72]  J. C. Middlebrooks,et al.  Location Coding by Opponent Neural Populations in the Auditory Cortex , 2005, PLoS biology.

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

[74]  P. Pohl Central auditory processing , 1983 .