Crossmodal plasticity in the fusiform gyrus of late blind individuals during voice recognition

Blind individuals are trained in identifying other people through voices. In congenitally blind adults the anterior fusiform gyrus has been shown to be active during voice recognition. Such crossmodal changes have been associated with a superiority of blind adults in voice perception. The key question of the present functional magnetic resonance imaging (fMRI) study was whether visual deprivation that occurs in adulthood is followed by similar adaptive changes of the voice identification system. Late blind individuals and matched sighted participants were tested in a priming paradigm, in which two voice stimuli were subsequently presented. The prime (S1) and the target (S2) were either from the same speaker (person-congruent voices) or from two different speakers (person-incongruent voices). Participants had to classify the S2 as either coming from an old or a young person. Only in late blind but not in matched sighted controls, the activation in the anterior fusiform gyrus was modulated by voice identity: late blind volunteers showed an increase of the BOLD signal in response to person-incongruent compared with person-congruent trials. These results suggest that the fusiform gyrus adapts to input of a new modality even in the mature brain and thus demonstrate an adult type of crossmodal plasticity.

[1]  A. Giraud,et al.  Implicit Multisensory Associations Influence Voice Recognition , 2006, PLoS biology.

[2]  Yang Dan,et al.  Experience-Dependent Plasticity in Adult Visual Cortex , 2006, Neuron.

[3]  Naomi B. Pitskel,et al.  Rapid and Reversible Recruitment of Early Visual Cortex for Touch , 2008, PloS one.

[4]  Leslie P. Keniston,et al.  Not Just for Bimodal Neurons Anymore: The Contribution of Unimodal Neurons to Cortical Multisensory Processing , 2009, Brain Topography.

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

[6]  C. Büchel,et al.  Brain systems mediating voice identity processing in blind humans , 2014, Human brain mapping.

[7]  Donald G. McLaren,et al.  Visual cortex activation in late-onset, Braille naive blind individuals: An fMRI study during semantic and phonological tasks with heard words , 2006, Neuroscience Letters.

[8]  N. Berman,et al.  Alterations of visual cortical connections in cats following early removal of retinal input. , 1991, Brain research. Developmental brain research.

[9]  R. Malach,et al.  Cortical activity during tactile exploration of objects in blind and sighted humans. , 2010, Restorative neurology and neuroscience.

[10]  C. Büchel,et al.  Corticocortical Connections Mediate Primary Visual Cortex Responses to Auditory Stimulation in the Blind , 2010, The Journal of Neuroscience.

[11]  D. Maurer,et al.  Effects of early pattern deprivation on visual development. , 2009, Optometry and vision science : official publication of the American Academy of Optometry.

[12]  Rebecca Saxe,et al.  Sensitive Period for a Multimodal Response in Human Visual Motion Area MT/MST , 2010, Current Biology.

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

[14]  R. Zatorre,et al.  Adaptation to speaker's voice in right anterior temporal lobe , 2003, Neuroreport.

[15]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[16]  Brigitte Röder,et al.  Crossmodal interaction of facial and vocal person identity information: An event-related potential study , 2011, Brain Research.

[17]  Lars Muckli,et al.  Cortical Plasticity of Audio–Visual Object Representations , 2008, Cerebral cortex.

[18]  C. Büchel,et al.  Increased amygdala activation to emotional auditory stimuli in the blind. , 2010, Brain : a journal of neurology.

[19]  Stefan J Kiebel,et al.  How the Human Brain Recognizes Speech in the Context of Changing Speakers , 2010, The Journal of Neuroscience.

[20]  D. Feldman Synaptic mechanisms for plasticity in neocortex. , 2009, Annual review of neuroscience.

[21]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[22]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[23]  R. Zatorre,et al.  Organization and Reorganization of Sensory-Deprived Cortex , 2012, Current Biology.

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

[25]  D. Hubel,et al.  The period of susceptibility to the physiological effects of unilateral eye closure in kittens , 1970, The Journal of physiology.

[26]  C. Gilbert,et al.  Adult Visual Cortical Plasticity , 2012, Neuron.

[27]  Anne-Lise Giraud,et al.  Distinct functional substrates along the right superior temporal sulcus for the processing of voices , 2004, NeuroImage.

[28]  P. Voss Sensitive and critical periods in visual sensory deprivation , 2013, Front. Psychol..

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

[30]  H. Burton,et al.  Dissociating cortical regions activated by semantic and phonological tasks: a FMRI study in blind and sighted people. , 2003, Journal of neurophysiology.

[31]  James M. McQueen,et al.  Neural mechanisms for voice recognition , 2010, NeuroImage.

[32]  M. Raichle,et al.  Adaptive changes in early and late blind: a FMRI study of verb generation to heard nouns. , 2002, Journal of neurophysiology.

[33]  T. James,et al.  An additive-factors design to disambiguate neuronal and areal convergence: measuring multisensory interactions between audio, visual, and haptic sensory streams using fMRI , 2009, Experimental Brain Research.

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

[35]  R. Zatorre,et al.  Voice perception in blind persons: A functional magnetic resonance imaging study , 2009, Neuropsychologia.

[36]  Joseph A Maldjian,et al.  Precentral gyrus discrepancy in electronic versions of the Talairach atlas , 2004, NeuroImage.

[37]  R J Ilmoniemi,et al.  Electrophysiological evidence for cross-modal plasticity in humans with early- and late-onset blindness. , 1997, Psychophysiology.

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

[39]  J C Mazziotta,et al.  Automated labeling of the human brain: A preliminary report on the development and evaluation of a forward‐transform method , 1997, Human brain mapping.

[40]  R. Henson Neuroimaging studies of priming , 2003, Progress in Neurobiology.

[41]  M. Hallett,et al.  Period of susceptibility for cross‐modal plasticity in the blind , 1999, Annals of neurology.

[42]  Anne G. De Volder,et al.  Cortical plasticity and preserved function in early blindness , 2014, Neuroscience & Biobehavioral Reviews.

[43]  Emiliano Ricciardi,et al.  Beyond sensory images: Object-based representation in the human ventral pathway. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Ryan A. Stevenson,et al.  Audiovisual integration in human superior temporal sulcus: Inverse effectiveness and the neural processing of speech and object recognition , 2009, NeuroImage.

[45]  U Yinon,et al.  Auditory activation of cortical visual areas in cats after early visual deprivation , 1999, The European journal of neuroscience.

[46]  E. Knudsen Sensitive Periods in the Development of the Brain and Behavior , 2004, Journal of Cognitive Neuroscience.

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

[48]  R. Saxe,et al.  A sensitive period for language in the visual cortex: Distinct patterns of plasticity in congenitally versus late blind adults , 2011, Brain and Language.

[49]  B. Clifford,et al.  The Voice-Recognition Accuracy of Blind Listeners , 1983, Perception.

[50]  Franco Lepore,et al.  Differential occipital responses in early- and late-blind individuals during a sound-source discrimination task , 2008, NeuroImage.

[51]  Karl J. Friston,et al.  The effect of prior visual information on recognition of speech and sounds. , 2008, Cerebral cortex.

[52]  D. Tomasi,et al.  Different activation patterns for working memory load and visual attention load , 2007, Brain Research.

[53]  Alfred Anwander,et al.  Direct Structural Connections between Voice- and Face-Recognition Areas , 2011, The Journal of Neuroscience.

[54]  Andreas Kleinschmidt,et al.  Interaction of Face and Voice Areas during Speaker Recognition , 2005, Journal of Cognitive Neuroscience.

[55]  Dylan M. Jones,et al.  Intra- and inter-modal repetition priming of familiar faces and voices. , 1997, British journal of psychology.

[56]  Jan Gläscher,et al.  Visualization of Group Inference Data in Functional Neuroimaging , 2009, Neuroinformatics.

[57]  L. Krubitzer,et al.  Early blindness results in abnormal corticocortical and thalamocortical connections , 2006, Neuroscience.

[58]  A. Kleinschmidt,et al.  Modulation of neural responses to speech by directing attention to voices or verbal content. , 2003, Brain research. Cognitive brain research.

[59]  Hartwig R. Siebner,et al.  The left fusiform gyrus hosts trisensory representations of manipulable objects , 2011, NeuroImage.

[60]  Ehud Zohary,et al.  Early ‘visual’ cortex activation correlates with superior verbal memory in the blind , 2003 .

[61]  G. Vandewalle,et al.  Impact of blindness onset on the functional organization and the connectivity of the occipital cortex. , 2013, Brain : a journal of neurology.

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

[63]  E. Zohary,et al.  Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects , 2004, Nature Neuroscience.

[64]  R. Zatorre,et al.  A positron emission tomography study during auditory localization by late-onset blind individuals , 2006, Neuroreport.

[65]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[66]  L. Maffei,et al.  Functional postnatal development of the rat primary visual cortex and the role of visual experience: Dark rearing and monocular deprivation , 1994, Vision Research.

[67]  D. Hubel,et al.  Extent of recovery from the effects of visual deprivation in kittens. , 1965, Journal of neurophysiology.

[68]  Leslie P. Keniston,et al.  Auditory influences on non-auditory cortices , 2009, Hearing Research.

[69]  B. Röder,et al.  The neural basis of lip-reading capabilities is altered by early visual deprivation , 2010, Neuropsychologia.

[70]  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.

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

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

[73]  Peter B. L. Meijer,et al.  Functional recruitment of visual cortex for sound encoded object identification in the blind , 2009, Neuroreport.