More accurate sound localization induced by short-term light deprivation

Crossmodal reorganization processes in the brain are mainly associated with early blindness, on the assumption that recruitment of genuine visual areas, such as primary visual cortex, for non-visual functions results in superior auditory and tactile performance of blind, compared to sighted, humans. This study shows that in sighted subjects the accuracy of sound localization, measured by a task of head pointing to acoustic targets, is reversibly increased after short-term light deprivation of 90 min. However, only the systematic deviations from target positions (constant error) were reduced after light deprivation, while the general precision of head pointing remained unchanged. Return to pre-deprivation values was observed after 180 min of re-exposure to light. The post-deprivation change was similar, though less in magnitude, to the effect of blindness that was demonstrated previously. Generally, these findings indicate that auditory-visual crossmodal plasticity can be quite rapidly initiated by deprivation of the visual cortex from visual input. It seems possible that visual deprivation has an influence on neuronal circuits, that are involved in processing of auditory information in visual brain areas of normal sighted humans. Since exclusively the constant error in sound localization, not general performance, was changed, the present effect of visual deprivation may, however, not be attributable to reorganization processes in the sense of a compensation for the absence of vision. It is more likely that the observed change in accuracy was specifically induced by the absence of visual calibration of the neural representation of auditory space during light deprivation.

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

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

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

[4]  Jörg Lewald,et al.  Visual and proprioceptive shifts in perceived egocentric direction induced by eye-position , 2000, Vision Research.

[5]  D. Ashmead,et al.  Sound localization and sensitivity to interaural time differences in human infants. , 1991, Child development.

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

[7]  Scott T. Grafton,et al.  Involvement of visual cortex in tactile discrimination of orientation , 1999, Nature.

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

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

[10]  Norihiro Sadato,et al.  Tactile discrimination activates the visual cortex of the recently blind naive to Braille: a functional magnetic resonance imaging study in humans , 2004, Neuroscience Letters.

[11]  Salvatore M. Aglioti,et al.  Short term light deprivation increases tactile spatial acuity in humans , 2003, Neurology.

[12]  M. Raichle,et al.  Adaptive changes in early and late blind: a fMRI study of Braille reading. , 2002, Journal of neurophysiology.

[13]  R. Ilmoniemi,et al.  Visual cortex activation in blind humans during sound discrimination , 1995, Neuroscience Letters.

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

[15]  Á. Pascual-Leone,et al.  Braille character discrimination in blindfolded human subjects , 2002, Neuroreport.

[16]  B. Röder,et al.  Influence of visual information on the auditory median plane of the head , 2002, Neuroreport.

[17]  C. L. Morgan Constancy of egocentric visual direction , 1978, Perception & psychophysics.

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

[19]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[20]  L. Cohen,et al.  Enhanced excitability of the human visual cortex induced by short-term light deprivation. , 2000, Cerebral cortex.

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

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

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

[24]  A. V. D. Berg,et al.  Perceived heading during simulated torsional eye movements , 2000, Vision Research.

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

[26]  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.

[27]  C. Spence,et al.  Early Vision Impairs Tactile Perception in the Blind , 2004, Current Biology.

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

[29]  C. Gilbert Adult cortical dynamics. , 1998, Physiological reviews.

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

[31]  J. Groh,et al.  Eye Position Affects Activity in Primary Auditory Cortex of Primates , 2003, Current Biology.

[32]  Á. Pascual-Leone,et al.  Tactile spatial resolution in blind Braille readers , 2000, Neurology.

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

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

[35]  David L. Sparks,et al.  Auditory receptive fields in primate superior colliculus shift with changes in eye position , 1984, Nature.

[36]  H. Burton Visual Cortex Activity in Early and Late Blind People , 2003, The Journal of Neuroscience.

[37]  M. Hallett,et al.  Neural networks for Braille reading by the blind. , 1998 .

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

[39]  R. Malach,et al.  Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind , 2003, Nature Neuroscience.

[40]  H Summala,et al.  Auditory processing in visual brain areas of the early blind: evidence from event-related potentials. , 1993, Electroencephalography and clinical neurophysiology.

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

[42]  Á. Pascual-Leone,et al.  Hearing with the minds eye , 2000, NeuroImage.

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

[44]  H. Burton,et al.  Cortical activity to vibrotactile stimulation: An fMRI study in blind and sighted individuals , 2004, Human brain mapping.

[45]  Karl J. Friston,et al.  Different activation patterns in the visual cortex of late and congenitally blind subjects. , 1998, Brain : a journal of neurology.

[46]  K Sathian,et al.  Feeling with the mind's eye: contribution of visual cortex to tactile perception , 2002, Behavioural Brain Research.

[47]  Ingrid M. Kanics,et al.  Tactile Acuity is Enhanced in Blindness , 2003, The Journal of Neuroscience.

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

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

[50]  W. Ehrenstein,et al.  Influence of head-to-trunk position on sound lateralization , 1998, Experimental Brain Research.

[51]  O. Bock,et al.  Contribution of retinal versus extraretinal signals towards visual localization in goal-directed movements , 2004, Experimental Brain Research.

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