Exceptional ability of blind humans to hear sound motion: Implications for the emergence of auditory space

Blind people may compensate for their visual loss by the increased use of auditory spatial information, thus showing normal or even supra-normal ability to localize sources of sound. However, the problem of how blind persons develop and maintain an internal concept of the topography of the auditory space in the absence of calibration by visual information is still unsolved. The present study demonstrated a substantial superiority of blind subjects in perception of auditory motion: The minimum audible movement angle of blind subjects (mean 3°) was about half the value found in matched sighted controls, whereas no such advantage was demonstrable for localization of stationary sound. There were no significant differences between early or congenitally blind subjects and late blind subjects, suggesting that long-term visual deprivation per se, independently of the point in time of its onset, was relevant for the superiority in auditory motion perception. The results were compatible with the hypothesis that in the absence of visual input the calibration of the auditory space is performed by audiomotor feedback, that is, by the evaluation of systematic changes of auditory spatial cues resulting from head and body movements. It is reasonable to assume that with blindness the neuronal circuits specifically concerned with the analysis of auditory motion are more intensely trained than in sighted people. It seems possible that the higher demand of motion analysis associated with blindness is related to processes of reorganization in the brain, as have been previously reported to occur also in areas known to be involved in auditory and/or visual motion analysis in sighted persons.

[1]  Fernando R Nodal,et al.  Training-Induced Plasticity of Auditory Localization in Adult Mammals , 2006, PLoS biology.

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

[3]  A Rees,et al.  Human brain areas involved in the analysis of auditory movement , 2000, Human brain mapping.

[4]  E I Knudsen,et al.  Vision guides the adjustment of auditory localization in young barn owls. , 1985, Science.

[5]  A. John Van Opstal,et al.  Plasticity in human sound localization induced by compressed spatial vision , 2003, Nature Neuroscience.

[6]  Jörg Lewald,et al.  Constancy of target velocity as a critical factor in the emergence of auditory and visual representational momentum , 2009, Experimental Brain Research.

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

[8]  D H Ashmead,et al.  Obstacle perception by congenitally blind children. , 1989, Perception & psychophysics.

[9]  B. Jones,et al.  Spatial perception in the blind. , 1975, British journal of psychology.

[10]  J. Lewald Rapid adaptation to auditory-visual spatial disparity. , 2002, Learning & memory.

[11]  G. Cioni,et al.  Role of vision on early motor development: lessons from the blind , 2001, Developmental medicine and child neurology.

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

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

[14]  D H Ashmead,et al.  Spatial Hearing in Children with Visual Disabilities , 1998, Perception.

[15]  Jörg Lewald,et al.  Effects of natural versus artificial spatial cues on electrophysiological correlates of auditory motion , 2010, Hearing Research.

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

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

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

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

[20]  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.

[21]  G. H. Fisher,et al.  SPATIAL LOCALIZATION BY THE BLIND. , 1964, The American journal of psychology.

[22]  J. Lewald,et al.  Processing of auditory motion in inferior parietal lobule: Evidence from transcranial magnetic stimulation , 2011, Neuropsychologia.

[23]  E I Knudsen,et al.  Vision-independent adjustment of unit tuning to sound localization cues in response to monaural occlusion in developing owl optic tectum , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  E. Knudsen,et al.  Mechanisms of experience-dependent plasticity in the auditory localization pathway of the barn owl , 1999, Journal of Comparative Physiology A.

[25]  Jörg Lewald,et al.  Localization of moving sound , 2007, Perception & psychophysics.

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

[27]  J. Lackner,et al.  Auditory cues for orientation and postural control in sighted and congenitally blind people , 1998, Experimental Brain Research.

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

[29]  J. Lewald,et al.  Allocentric or Craniocentric Representation of Acoustic Space: An Electrotomography Study Using Mismatch Negativity , 2012, PloS one.

[30]  Jörg Lewald,et al.  Eye-position effects in directional hearing , 1997, Behavioural Brain Research.

[31]  Alexander G. Huth,et al.  Visual Motion Area MT+/V5 Responds to Auditory Motion in Human Sight-Recovery Subjects , 2008, The Journal of Neuroscience.

[32]  Jörg Lewald,et al.  Sound localization with eccentric head position , 2000, Behavioural Brain Research.

[33]  S. Getzmann,et al.  Representational momentum in spatial hearing does not depend on eye movements , 2005, Experimental Brain Research.

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

[35]  R. Zatorre,et al.  Relevance of Spectral Cues for Auditory Spatial Processing in the Occipital Cortex of the Blind , 2011, Front. Psychology.

[36]  R Kalil,et al.  Compensation for Auditory Re-Arrangement in the Absence of Observer Movement , 1967, Perceptual and motor skills.

[37]  W Pieter Medendorp,et al.  Rotational Remapping in Human Spatial Memory during Eye and Head Motion , 2002, The Journal of Neuroscience.

[38]  Jonathan Z. Simon,et al.  A Sensorimotor Approach to Sound Localization , 2008, Neural Computation.

[39]  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.

[40]  M. Wertheimer Psychomotor Coordination of Auditory and Visual Space at Birth , 1961, Science.

[41]  E. Knudsen,et al.  Vision calibrates sound localization in developing barn owls , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[43]  G. Recanzone Rapidly induced auditory plasticity: the ventriloquism aftereffect. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[44]  E. Knudsen,et al.  Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[47]  L. K. Canon,et al.  Directed attention and maladaptive "adaptation" to displacement of the visual field. , 1971, Journal of experimental psychology.

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

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

[50]  J Field,et al.  Newborn infants orient to sounds. , 1979, Child development.

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

[52]  M. Corballis,et al.  Perception of stationary and moving sound following unilateral cortectomy , 2009, Neuropsychologia.

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

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

[55]  R. Held Shifts in binaural localization after prolonged exposures to atypical combinations of stimuli. , 1955, The American journal of psychology.

[56]  Steven A. Hillyard,et al.  Auditory Spatial Tuning in Late-onset Blindness in Humans , 2006, Journal of Cognitive Neuroscience.

[57]  Andrew J. King,et al.  Visual influences on auditory spatial learning , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.