Reorganization of Sound Location Processing in the Auditory Cortex of Blind Humans.

Auditory spatial tasks induce functional activation in the occipital-visual-cortex of early blind humans. Less is known about the effects of blindness on auditory spatial processing in the temporal-auditory-cortex. Here, we investigated spatial (azimuth) processing in congenitally and early blind humans with a phase-encoding functional magnetic resonance imaging (fMRI) paradigm. Our results show that functional activation in response to sounds in general-independent of sound location-was stronger in the occipital cortex but reduced in the medial temporal cortex of blind participants in comparison with sighted participants. Additionally, activation patterns for binaural spatial processing were different for sighted and blind participants in planum temporale. Finally, fMRI responses in the auditory cortex of blind individuals carried less information on sound azimuth position than those in sighted individuals, as assessed with a 2-channel, opponent coding model for the cortical representation of sound azimuth. These results indicate that early visual deprivation results in reorganization of binaural spatial processing in the auditory cortex and that blind individuals may rely on alternative mechanisms for processing azimuth position.

[1]  Giancarlo Valente,et al.  Active Sound Localization Sharpens Spatial Tuning in Human Primary Auditory Cortex , 2018, The Journal of Neuroscience.

[2]  A. Rees,et al.  Auditory motion-specific mechanisms in the primate brain , 2017, PLoS biology.

[3]  Ione Fine,et al.  Early Blindness Results in Developmental Plasticity for Auditory Motion Processing within Auditory and Occipital Cortex , 2016, Front. Hum. Neurosci..

[4]  Franco Lepore,et al.  Auditory motion in the sighted and blind: Early visual deprivation triggers a large-scale imbalance between auditory and “visual” brain regions , 2016, NeuroImage.

[5]  E. Formisano,et al.  Opponent Coding of Sound Location (Azimuth) in Planum Temporale is Robust to Sound-Level Variations , 2015, Cerebral cortex.

[6]  Thomas E. Nichols,et al.  Can parametric statistical methods be trusted for fMRI based group studies? , 2015, 1511.01863.

[7]  Robert J Zatorre,et al.  Trade-Off in the Sound Localization Abilities of Early Blind Individuals between the Horizontal and Vertical Planes , 2015, The Journal of Neuroscience.

[8]  Ione Fine,et al.  Auditory motion processing after early blindness. , 2014, Journal of vision.

[9]  E. Naito,et al.  Efficient foot motor control by Neymar’s brain , 2014, Front. Hum. Neurosci..

[10]  Rainer Goebel,et al.  Functionally informed cortex based alignment: An integrated approach for whole-cortex macro-anatomical and ROI-based functional alignment , 2013, NeuroImage.

[11]  A. Cowey,et al.  Early Auditory Processing in Area V5/MT+ of the Congenitally Blind Brain , 2013, The Journal of Neuroscience.

[12]  Jörg Lewald,et al.  Exceptional ability of blind humans to hear sound motion: Implications for the emergence of auditory space , 2013, Neuropsychologia.

[13]  Pavel Zahorik,et al.  Decoding the direction of auditory motion in blind humans , 2011, NeuroImage.

[14]  Amir Amedi,et al.  Extensive Cochleotopic Mapping of Human Auditory Cortical Fields Obtained with Phase-Encoding fMRI , 2011, PloS one.

[15]  G. Vandewalle,et al.  Functional specialization for auditory–spatial processing in the occipital cortex of congenitally blind humans , 2011, Proceedings of the National Academy of Sciences.

[16]  Wietske van der Zwaag,et al.  Where sound position influences sound object representations: A 7-T fMRI study , 2011, NeuroImage.

[17]  J. Rauschecker,et al.  Preserved Functional Specialization for Spatial Processing in the Middle Occipital Gyrus of the Early Blind , 2010, Neuron.

[18]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[19]  M. Rushworth,et al.  Behavioral / Systems / Cognitive Connectivity-Based Parcellation of Human Cingulate Cortex and Its Relation to Functional Specialization , 2008 .

[20]  Kurt E. Weaver,et al.  Functional characteristics of auditory cortex in the blind , 2009, Behavioural Brain Research.

[21]  Jörg Lewald,et al.  More accurate sound localization induced by short-term light deprivation , 2007, Neuropsychologia.

[22]  Robert T. Knight,et al.  Cerebral Responses to Change in Spatial Location of Unattended Sounds , 2007, Neuron.

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

[24]  Colline Poirier,et al.  Auditory motion perception activates visual motion areas in early blind subjects , 2006, NeuroImage.

[25]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

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

[27]  G L Romani,et al.  Human brain activation during passive listening to sounds from different locations: An fMRI and MEG study , 2005, Human brain mapping.

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

[29]  Nadim Joni Shah,et al.  Cortical Representations of Personally Familiar Objects and Places: Functional Organization of the Human Posterior Cingulate Cortex , 2005, Journal of Cognitive Neuroscience.

[30]  R. Zatorre,et al.  A Functional Neuroimaging Study of Sound Localization: Visual Cortex Activity Predicts Performance in Early-Blind Individuals , 2005, PLoS biology.

[31]  Franco Lepore,et al.  Early- and Late-Onset Blind Individuals Show Supra-Normal Auditory Abilities in Far-Space , 2004, Current Biology.

[32]  R. Zatorre,et al.  Neuropsychology: Pitch discrimination in the early blind , 2004, Nature.

[33]  T. Wüstenberg,et al.  Long-term training affects cerebellar processing in skilled keyboard players , 2004, Neuroreport.

[34]  M. Harms,et al.  Detection and quantification of a wide range of fMRI temporal responses using a physiologically‐motivated basis set , 2003, Human brain mapping.

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

[36]  Todd B. Parrish,et al.  The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention , 2003, NeuroImage.

[37]  Jörg Lewald,et al.  Vertical sound localization in blind humans , 2002, Neuropsychologia.

[38]  Matthias M. Müller,et al.  Expansion of the Tonotopic Area in the Auditory Cortex of the Blind , 2002, The Journal of Neuroscience.

[39]  John G. Neuhoff,et al.  Spatiotemporal Pattern of Neural Processing in the Human Auditory Cortex , 2002, Science.

[40]  M. Harms,et al.  Sound repetition rate in the human auditory pathway: representations in the waveshape and amplitude of fMRI activation. , 2002, Journal of neurophysiology.

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

[42]  Jörg Lewald,et al.  Opposing effects of head position on sound localization in blind and sighted human subjects , 2002, The European journal of neuroscience.

[43]  J. Cruysberg,et al.  Two-dimensional sound-localization behavior of early-blind humans , 2001, Experimental Brain Research.

[44]  M. P. Zwiers,et al.  A Spatial Hearing Deficit in Early-Blind Humans , 2001, The Journal of Neuroscience.

[45]  L. Jäncke,et al.  Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists. , 2000, Brain research. Cognitive brain research.

[46]  Daniel S. O'Leary,et al.  An MRI-Based Parcellation Method for the Temporal Lobe , 2000, NeuroImage.

[47]  J. Rauschecker,et al.  A Positron Emission Tomographic Study of Auditory Localization in the Congenitally Blind , 2000, The Journal of Neuroscience.

[48]  A J King,et al.  Improved auditory spatial acuity in visually deprived ferrets , 1999, The European journal of neuroscience.

[49]  S. Hillyard,et al.  Improved auditory spatial tuning in blind humans , 1999, Nature.

[50]  A. David,et al.  The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance , 1999, Brain Research Reviews.

[51]  M. Paré,et al.  Early-blind human subjects localize sound sources better than sighted subjects , 1998, Nature.

[52]  C. Leonard,et al.  Normal variation in the frequency and location of human auditory cortex landmarks. Heschl's gyrus: where is it? , 1998, Cerebral cortex.

[53]  M. Hallett,et al.  Functional relevance of cross-modal plasticity in blind humans , 1997, Nature.

[54]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[55]  F. Rösler,et al.  Event-related potentials during auditory and somatosensory discrimination in sighted and blind human subjects. , 1996, Brain research. Cognitive brain research.

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

[57]  J. Rauschecker,et al.  Auditory Localization Behaviour in Visually Deprived Cats , 1994, The European journal of neuroscience.

[58]  J. Rauschecker,et al.  Auditory spatial tuning of cortical neurons is sharpened in cats with early blindness. , 1993, Journal of neurophysiology.

[59]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

[60]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[61]  Simon R. Oldfield,et al.  Acuity of Sound Localisation: A Topography of Auditory Space. I. Normal Hearing Conditions , 1984, Perception.

[62]  Simon R. Oldfield,et al.  Acuity of Sound Localisation: A Topography of Auditory Space. II. Pinna Cues Absent , 1984, Perception.

[63]  J. Minckler,et al.  A note on the gross configurations of the human auditory cortex , 1976, Brain and Language.

[64]  R. Fisher.  FREQUENCY DISTRIBUTION OF THE VALUES OF THE CORRELATION COEFFIENTS IN SAMPLES FROM AN INDEFINITELY LARGE POPU;ATION , 1915 .

[65]  F. Gall.  Functional Specialization , 2021, Encyclopedia of Evolutionary Psychological Science.

[66]  J. Rauschecker.  Early Auditory Processing , 2015 .

[67]  L. Merabet,et al.  Neural reorganization following sensory loss: the opportunity of change , 2010, Nature Reviews Neuroscience.

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

[69]  Vladimir N. Vapnik,et al.  The Nature of Statistical Learning Theory , 2000, Statistics for Engineering and Information Science.

[70]  S. Telles,et al.  Shorter latencies of components of middle latency auditory evoked potentials in congenitally blind compared to normal sighted subjects. , 1998, The International journal of neuroscience.

[71]  A D Musicant,et al.  Influence of monaural spectral cues on binaural localization. , 1985, The Journal of the Acoustical Society of America.