Adaptation of the communicative brain to post-lingual deafness. Evidence from functional imaging

Not having access to one sense profoundly modifies our interactions with the environment, in turn producing changes in brain organization. Deafness and its rehabilitation by cochlear implantation offer a unique model of brain adaptation during sensory deprivation and recovery. Functional imaging allows the study of brain plasticity as a function of the times of deafness and implantation. Even long after the end of the sensitive period for auditory brain physiological maturation, some plasticity may be observed. In this way the mature brain that becomes deaf after language acquisition can adapt to its modified sensory inputs. Oral communication difficulties induced by post-lingual deafness shape cortical reorganization of brain networks already specialized for processing oral language. Left hemisphere language specialization tends to be more preserved than functions of the right hemisphere. We hypothesize that the right hemisphere offers cognitive resources re-purposed to palliate difficulties in left hemisphere speech processing due to sensory and auditory memory degradation. If cochlear implantation is considered, this reorganization during deafness may influence speech understanding outcomes positively or negatively. Understanding brain plasticity during post-lingual deafness should thus inform the development of cognitive rehabilitation, which promotes positive reorganization of the brain networks that process oral language before surgery. This article is part of a Special Issue entitled Human Auditory Neuroimaging.

[1]  Ruth Campbell,et al.  Sign language and the brain: a review. , 2008, Journal of deaf studies and deaf education.

[2]  D. Abrams,et al.  Right-Hemisphere Auditory Cortex Is Dominant for Coding Syllable Patterns in Speech , 2008, The Journal of Neuroscience.

[3]  Olivier Deguine,et al.  Multisensory Processing in Cochlear Implant Listeners , 2011 .

[4]  D. Poeppel,et al.  Speech perception at the interface of neurobiology and linguistics , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  R. Shannon,et al.  Speech recognition in noise as a function of the number of spectral channels: comparison of acoustic hearing and cochlear implants. , 2001, The Journal of the Acoustical Society of America.

[6]  Ione Fine,et al.  Visual stimuli activate auditory cortex in the deaf , 2001, Nature Neuroscience.

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

[8]  Kayoko Okada,et al.  Bilateral capacity for speech sound processing in auditory comprehension: Evidence from Wada procedures , 2008, Brain and Language.

[9]  Eric Truy,et al.  Bilateral reorganization of posterior temporal cortices in post‐lingual deafness and its relation to cochlear implant outcome , 2013, Human brain mapping.

[10]  Noam Chomsky,et al.  The Sound Pattern of English , 1968 .

[11]  I. Johnsrude,et al.  Spectral and temporal processing in human auditory cortex. , 2002, Cerebral cortex.

[12]  Andrej Kral,et al.  Unimodal and cross-modal plasticity in the ‘deaf’ auditory cortex , 2007, International journal of audiology.

[13]  K. Hugdahl,et al.  Lateralization of cognitive processes in the brain. , 2000, Acta psychologica.

[14]  Hyejin Kang,et al.  Preoperative differences of cerebral metabolism relate to the outcome of cochlear implants in congenitally deaf children , 2005, Hearing Research.

[15]  A. Beynon,et al.  Factors Affecting Auditory Performance of Postlinguistically Deaf Adults Using Cochlear Implants: An Update with 2251 Patients , 2012, Audiology and Neurotology.

[16]  J. Eggermont The Role of Sound in Adult and Developmental Auditory Cortical Plasticity , 2008, Ear and hearing.

[17]  Richard S. J. Frackowiak,et al.  Cross-Modal Plasticity Underpins Language Recovery after Cochlear Implantation , 2001, Neuron.

[18]  Andrej Kral,et al.  Profound deafness in childhood. , 2010, The New England journal of medicine.

[19]  William W. Graves,et al.  Neural Systems for Reading Aloud: A Multiparametric Approach , 2009, Cerebral cortex.

[20]  M. Dorman,et al.  Deprivation-induced cortical reorganization in children with cochlear implants , 2007, International journal of audiology.

[21]  Michael Forsting,et al.  Cross-modal plasticity in deaf subjects dependent on the extent of hearing loss. , 2005, Brain research. Cognitive brain research.

[22]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[23]  F B Simmons,et al.  Electrical stimulation of the auditory nerve in man. , 1966, Archives of otolaryngology.

[24]  B. Argall,et al.  Integration of Auditory and Visual Information about Objects in Superior Temporal Sulcus , 2004, Neuron.

[25]  Helen J. Neville,et al.  Attention to central and peripheral visual space in a movement detection task: an event-related potential and behavioral study. I. Normal hearing adults , 1987, Brain Research.

[26]  D. Proops,et al.  Criteria of Candidacy for Unilateral Cochlear Implantation in Postlingually Deafened Adults I: Theory and Measures of Effectiveness , 2004, Ear and hearing.

[27]  Philipos C Loizou,et al.  Speech processing in vocoder-centric cochlear implants. , 2006, Advances in oto-rhino-laryngology.

[28]  M. Lassonde,et al.  Cross-modal reorganization and speech perception in cochlear implant users. , 2006, Brain : a journal of neurology.

[29]  P. Barone,et al.  Evolution of crossmodal reorganization of the voice area in cochlear‐implanted deaf patients , 2012, Human brain mapping.

[30]  Craig J. Brozinsky,et al.  Impact of Early Deafness and Early Exposure to Sign Language on the Cerebral Organization for Motion Processing , 2001, The Journal of Neuroscience.

[31]  Matthew W. G. Dye,et al.  Do deaf individuals see better? , 2006, Trends in Cognitive Sciences.

[32]  B Fraysse,et al.  Does brain activity at rest reflect adaptive strategies? Evidence from speech processing after cochlear implantation. , 2010, Cerebral cortex.

[33]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[34]  Christine Preibisch,et al.  Evidence for compensation for stuttering by the right frontal operculum , 2003, NeuroImage.

[35]  Robert V. Shannon,et al.  Multichannel electrical stimulation of the auditory nerve in man. II. Channel interaction , 1983, Hearing Research.

[36]  Brian C J Moore,et al.  Speech perception problems of the hearing impaired reflect inability to use temporal fine structure , 2006, Proceedings of the National Academy of Sciences.

[37]  Helen J. Neville,et al.  Attention to central and peripheral visual space in a movement detection task: an event-related potential and behavioral study. II. Congenitally deaf adults , 1987, Brain Research.

[38]  D. Lazard,et al.  Speech processing: From peripheral to hemispheric asymmetry of the auditory system , 2012, The Laryngoscope.

[39]  Jeffrey R Binder,et al.  Human brain regions involved in recognizing environmental sounds. , 2004, Cerebral cortex.

[40]  Ione Fine,et al.  Comparing the Effects of Auditory Deprivation and Sign Language within the Auditory and Visual Cortex , 2005, Journal of Cognitive Neuroscience.

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

[42]  P. Barone,et al.  Role of speechreading in audiovisual interactions during the recovery of speech comprehension in deaf adults with cochlear implants. , 2009, Scandinavian journal of psychology.

[43]  Robert J Zatorre,et al.  Neural specializations for speech and pitch: moving beyond the dichotomies , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  H. Coslett,et al.  Localization of sublexical speech perception components , 2010, Brain and Language.

[45]  Anne-Lise Giraud,et al.  How the brain repairs stuttering. , 2009, Brain : a journal of neurology.

[46]  D. Pisoni,et al.  PET imaging of cochlear-implant and normal-hearing subjects listening to speech and nonspeech , 1999, Hearing Research.

[47]  Hyo-Jeong Lee,et al.  Predicting cochlear implant outcome from brain organisation in the deaf. , 2007, Restorative neurology and neuroscience.

[48]  Eric Halgren,et al.  Sequential Processing of Lexical, Grammatical, and Phonological Information Within Broca’s Area , 2009, Science.

[49]  Y. Yonekura,et al.  Cortical activation with sound stimulation in cochlear implant users demonstrated by positron emission tomography. , 1995, Brain research. Cognitive brain research.

[50]  A. Beynon,et al.  Pre-, Per- and Postoperative Factors Affecting Performance of Postlinguistically Deaf Adults Using Cochlear Implants: A New Conceptual Model over Time , 2012, PloS one.

[51]  Kayoko Okada,et al.  Area Spt in the Human Planum Temporale Supports Sensory-motor Integration for Speech Processing Establishing the Existence of Distinct Sen- Sory versus Motor Activation Patterns Would Establish That , 2022 .

[52]  P. Barone,et al.  Visual activity predicts auditory recovery from deafness after adult cochlear implantation. , 2013, Brain : a journal of neurology.

[53]  Á. Pascual-Leone,et al.  Improved picture naming in chronic aphasia after TMS to part of right Broca’s area: An open-protocol study , 2005, Brain and Language.

[54]  Argye E Hillis,et al.  Recovery from aphasia following brain injury: the role of reorganization. , 2006, Progress in brain research.

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

[56]  Brigitte Röder,et al.  Compensatory Plasticity as a Consequence of Sensory Loss. , 2004 .

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

[58]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[59]  T. Sanger,et al.  Harnessing neuroplasticity for clinical applications , 2011, Brain : a journal of neurology.

[60]  Michael Dorman,et al.  Cortical development, plasticity and re-organization in children with cochlear implants. , 2009, Journal of communication disorders.

[61]  J. Eggermont,et al.  What's to lose and what's to learn: Development under auditory deprivation, cochlear implants and limits of cortical plasticity , 2007, Brain Research Reviews.

[62]  J. A. Frost,et al.  Function of the left planum temporale in auditory and linguistic processing , 1996, NeuroImage.

[63]  G Jobard,et al.  Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies , 2003, NeuroImage.

[64]  A. Giraud,et al.  Cortical activity at rest predicts cochlear implantation outcome. , 2007, Cerebral cortex.

[65]  C. Price,et al.  The Interactive Account of ventral occipitotemporal contributions to reading , 2011, Trends in Cognitive Sciences.

[66]  Matthew W. G. Dye,et al.  Attentional enhancements and deficits in deaf populations: an integrative review. , 2010, Restorative neurology and neuroscience.

[67]  S. Dehaene,et al.  Functional Neuroimaging of Speech Perception in Infants , 2002, Science.

[68]  J. Besle,et al.  The effect of long-term unilateral deafness on the activation pattern in the auditory cortices of French-native speakers: influence of deafness side , 2009, BMC Neuroscience.

[69]  Philip K. McGuire,et al.  Neural Correlates of British Sign Language Comprehension: Spatial Processing Demands of Topographic Language , 2002, Journal of Cognitive Neuroscience.

[70]  L Whitford,et al.  Factors affecting auditory performance of postlinguistically deaf adults using cochlear implants. , 1996, Audiology & neuro-otology.

[71]  Eric Truy,et al.  Visual speech circuits in profound acquired deafness: a possible role for latent multimodal connectivity. , 2007, Brain : a journal of neurology.

[72]  Albert Gjedde,et al.  Restored speech comprehension linked to activity in left inferior prefrontal and right temporal cortices in postlingual deafness , 2006, NeuroImage.

[73]  B. Fraysse,et al.  Evidence that cochlear-implanted deaf patients are better multisensory integrators , 2007, Proceedings of the National Academy of Sciences.

[74]  C. Fiebach,et al.  fMRI Evidence for Dual Routes to the Mental Lexicon in Visual Word Recognition , 2002, Journal of Cognitive Neuroscience.

[75]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[76]  Nick F. Ramsey,et al.  Contribution of the left and right inferior frontal gyrus in recovery from aphasia. A functional MRI study in stroke patients with preserved hemodynamic responsiveness , 2010, NeuroImage.

[77]  Hans-Jochen Heinze,et al.  Scanning silence: Mental imagery of complex sounds , 2005, NeuroImage.

[78]  C Pantev,et al.  Dynamics of auditory plasticity after cochlear implantation: a longitudinal study. , 2006, Cerebral cortex.

[79]  S. Levänen,et al.  Vibration-induced auditory-cortex activation in a congenitally deaf adult , 1998, Current Biology.

[80]  Michael Gaebler,et al.  Phonological processing in post-lingual deafness and cochlear implant outcome , 2010, NeuroImage.

[81]  Hyo-Jeong Lee,et al.  Speech experience shapes the speechreading network and subsequent deafness facilitates it. , 2009, Brain : a journal of neurology.

[82]  Rainer Goebel,et al.  "Who" Is Saying "What"? Brain-Based Decoding of Human Voice and Speech , 2008, Science.

[83]  Andrej Kral,et al.  Developmental neuroplasticity after cochlear implantation , 2012, Trends in Neurosciences.

[84]  K E Spens,et al.  Cognitive correlates of visual speech understanding in hearing-impaired individuals. , 2001, Journal of deaf studies and deaf education.

[85]  西村 洋 Sign language "heard"in the auditory cortex , 2000 .

[86]  S. Debener,et al.  Visual activation of auditory cortex reflects maladaptive plasticity in cochlear implant users. , 2012, Brain : a journal of neurology.

[87]  Paul C. Locasto,et al.  A systematic investigation of the functional neuroanatomy of auditory and visual phonological processing , 2005, NeuroImage.

[88]  J. Eggermont,et al.  Maturational delays in cortical evoked potentials in cochlear implant users. , 1997, Acta oto-laryngologica.

[89]  P. Julyan,et al.  Auditory cortical activation and speech perception in cochlear implant users: Effects of implant experience and duration of deafness , 2005, Hearing Research.

[90]  Karl J. Friston Modalities, Modes, and Models in Functional Neuroimaging , 2009, Science.

[91]  André Syrota,et al.  Cochlear Implant Benefits in Deafness Rehabilitation: PET Study of Temporal Voice Activations , 2007, Journal of Nuclear Medicine.

[92]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[93]  J. Rauschecker Compensatory plasticity and sensory substitution in the cerebral cortex , 1995, Trends in Neurosciences.

[94]  E. Truyc,et al.  Evolution of non-speech sound memory in postlingual deafness : implications for cochlear implant rehabilitation , 2016 .

[95]  Neural plasticity detected in short‐and long‐term cochlear implant users using PET , 2000, Neuroreport.