Temporal cues trick the visual and auditory cortices mimicking spatial cues in blind individuals

In the absence of vision, spatial representation may be altered. When asked to compare the relative distances between three sounds (i.e., auditory spatial bisection task), blind individuals demonstrate significant deficits and do not show an event‐related potential response mimicking the visual C1 reported in sighted people. However, we have recently demonstrated that the spatial deficit disappears if coherent time and space cues are presented to blind people, suggesting that they may use time information to infer spatial maps. In this study, we examined whether the modification of temporal cues during space evaluation altered the recruitment of the visual and auditory cortices in blind individuals. We demonstrated that the early (50–90 ms) occipital response, mimicking the visual C1, is not elicited by the physical position of the sound, but by its virtual position suggested by its temporal delay. Even more impressively, in the same time window, the auditory cortex also showed this pattern and responded to temporal instead of spatial coordinates.

[1]  A. King,et al.  Sound localization in a changing world , 2015, Current Opinion in Neurobiology.

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

[3]  M. Bedny,et al.  “Visual” Cortex of Congenitally Blind Adults Responds to Syntactic Movement , 2015, The Journal of Neuroscience.

[4]  Andrew J. Kolarik,et al.  Evidence for enhanced discrimination of virtual auditory distance among blind listeners using level and direct-to-reverberant cues , 2012, Experimental Brain Research.

[5]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[6]  Franco Lepore,et al.  Wayfinding in the blind: larger hippocampal volume and supranormal spatial navigation. , 2008, Brain : a journal of neurology.

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

[8]  D. Burr,et al.  Auditory dominance over vision in the perception of interval duration , 2009, Experimental Brain Research.

[9]  Maria Bianca Amadeo,et al.  Impact of years of blindness on neural circuits underlying auditory spatial representation , 2019, NeuroImage.

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

[11]  Matthias M. Müller,et al.  Perceptual Correlates of Changes in Cortical Representation of Fingers in Blind Multifinger Braille Readers , 1998, The Journal of Neuroscience.

[12]  B. Röder,et al.  The superiority in voice processing of the blind arises from neural plasticity at sensory processing stages , 2012, Neuropsychologia.

[13]  Viola S. Störmer,et al.  Salient Sounds Activate Human Visual Cortex Automatically , 2013, The Journal of Neuroscience.

[14]  Maria Concetta Morrone,et al.  Spatiotopic coding and remapping in humans , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[15]  F. Rösler,et al.  Speech processing activates visual cortex in congenitally blind humans , 2002, The European journal of neuroscience.

[16]  Maria Bianca Amadeo,et al.  Temporal Cues Influence Space Estimations in Visually Impaired Individuals , 2018, iScience.

[17]  M. Ernst,et al.  Signal reliability modulates auditory–tactile integration for event counting , 2007, Neuroreport.

[18]  Maria Bianca Amadeo,et al.  Stronger responses in the visual cortex of sighted compared to blind individuals during auditory space representation , 2019, Scientific Reports.

[19]  Tobias S. Andersen,et al.  Classification of independent components of EEG into multiple artifact classes. , 2015, Psychophysiology.

[20]  G. Sandini,et al.  Development of Visuo-Auditory Integration in Space and Time , 2012, Front. Integr. Neurosci..

[21]  Jennifer M. Groh,et al.  Making Space: How the Brain Knows Where Things Are , 2014 .

[22]  G. Sandini,et al.  Impairment of auditory spatial localization in congenitally blind human subjects , 2013, Brain : a journal of neurology.

[23]  S. Shimojo,et al.  Sound alters visual evoked potentials in humans , 2001, Neuroreport.

[24]  K. Alho,et al.  Auditory and somatosensory event-related brain potentials in early blind humans , 2004, Experimental Brain Research.

[25]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[26]  C. Blakemore,et al.  Developmental plasticity in the visual and auditory representations in the mammalian superior colliculus , 1988, Nature.

[27]  John J. Foxe,et al.  Human–simian correspondence in the early cortical processing of multisensory cues , 2004, Cognitive Processing.

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

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

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

[31]  S. Carlile,et al.  Changes induced in the representation of auditory space in the superior colliculus by rearing ferrets with binocular eyelid suture , 2004, Experimental Brain Research.

[32]  S. Shimojo,et al.  Illusions: What you see is what you hear , 2000, Nature.

[33]  Brigitte Röder,et al.  Attending points in time and space , 2006, Experimental Brain Research.

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

[35]  Brian C. J. Moore,et al.  Auditory spatial representations of the world are compressed in blind humans , 2016, Experimental Brain Research.

[36]  Andrew J. King,et al.  What happens to your hearing if you are born blind? , 2014, Brain : a journal of neurology.

[37]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

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

[39]  K. H. Stauder,et al.  Psychology of the Child , 1959 .

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

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

[42]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.

[43]  Tzyy-Ping Jung,et al.  Real-time modeling and 3D visualization of source dynamics and connectivity using wearable EEG , 2013, 2013 35th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

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

[45]  D. Burr,et al.  Early visual deprivation severely compromises the auditory sense of space in congenitally blind children. , 2016, Developmental psychology.

[46]  Jong Doo Lee,et al.  Morphological alterations in the congenital blind based on the analysis of cortical thickness and surface area , 2009, NeuroImage.

[47]  Dorothy V. M. Bishop,et al.  Journal of Neuroscience Methods , 2015 .

[48]  C Veraart,et al.  Processing of auditory information by the blind in spatial localization tasks , 1985, Perception & psychophysics.

[49]  William M. Stern,et al.  Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex , 2007, Nature Neuroscience.

[50]  R. Saxe,et al.  Language processing in the occipital cortex of congenitally blind adults , 2011, Proceedings of the National Academy of Sciences.

[51]  John J. Foxe,et al.  The Spatiotemporal Dynamics of Illusory Contour Processing: Combined High-Density Electrical Mapping, Source Analysis, and Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[52]  Marco Tamietto,et al.  Visual Experience is not Necessary for Efficient Survey Spatial Cognition: Evidence from Blindness , 2006, Quarterly journal of experimental psychology.

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

[54]  Geraint Rees,et al.  Sound alters activity in human V1 in association with illusory visual perception , 2006, NeuroImage.

[55]  Monica Gori,et al.  Spatial localization of sound elicits early responses from occipital visual cortex in humans , 2017, Scientific Reports.

[56]  T. Picton,et al.  The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. , 1987, Psychophysiology.

[57]  Jean Piaget,et al.  The child's conception of time; , 1969 .

[58]  M. Gori Multisensory Integration and Calibration in Children and Adults with and without Sensory and Motor Disabilities. , 2015, Multisensory research.

[59]  B. Jones,et al.  On the interdependence of temporal and spatial judgments , 1982, Perception & psychophysics.

[60]  David J. Heeger,et al.  Neuronal correlates of perception in early visual cortex , 2003, Nature Neuroscience.