Functional Near-Infrared Spectroscopy Brain Imaging Investigation of Phonological Awareness and Passage Comprehension Abilities in Adult Recipients of Cochlear Implants.

PURPOSE The aim of this study was to examine how the brains of individuals with cochlear implants (CIs) respond to spoken language tasks that underlie successful language acquisition and processing. METHOD During functional near-infrared spectroscopy imaging, CI recipients with hearing impairment (n = 10, mean age: 52.7 ± 17.3 years) and controls with normal hearing (n = 10, mean age: 50.6 ± 17.2 years) completed auditory tasks-phonological awareness and passage comprehension-commonly used to investigate neurodevelopmental disorders of language and literacy. RESULTS The 2 groups had similar reaction time and performance on experimental tasks, although participants with CIs had lower accuracy than controls. Overall, both CI recipients and controls exhibited similar patterns of brain activation during the tasks. CONCLUSIONS The results demonstrate that CI recipients show an overall neurotypical pattern of activation during auditory language tasks on which individuals with neurodevelopmental language learning impairments (e.g., dyslexia) tend to show atypical brain activation. These findings suggest that advancements in functional near-infrared spectroscopy neuroimaging with CI recipients may help shed new light on how varying types of difficulties in language processing affect brain organization for language.

[1]  Ioulia Kovelman,et al.  At the rhythm of language: Brain bases of language-related frequency perception in children , 2012, NeuroImage.

[2]  S E Petersen,et al.  Detection of cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[3]  P. Vuust,et al.  Cortical Plasticity after Cochlear Implantation , 2013, Neural plasticity.

[4]  R. Poldrack,et al.  Disrupted neural responses to phonological and orthographic processing in dyslexic children: an fMRI study , 2001, Neuroreport.

[5]  M. Hildesheimer,et al.  Phonetic Processing in Children With Cochlear Implants: An Auditory Event-Related Potentials Study , 2008, Ear and hearing.

[6]  Paul Boersma,et al.  Praat: doing phonetics by computer , 2003 .

[7]  Isabell Wartenburger,et al.  Early Setting of Grammatical Processing in the Bilingual Brain , 2003, Neuron.

[8]  Jamie Zibulsky,et al.  Clinical Evaluation of Language Fundamentals, Fourth Edition , 2014 .

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

[10]  B. Satar,et al.  Evaluation of cochlear implant users’ performance using middle and late latency responses , 2009, European Archives of Oto-Rhino-Laryngology.

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

[12]  Blake C Papsin,et al.  Atypical cortical responses underlie poor speech perception in children using cochlear implants , 2005, Neuroreport.

[13]  A. Morgan,et al.  Neural correlates of childhood language disorder: a systematic review , 2015, Developmental medicine and child neurology.

[14]  I. Kovelman,et al.  Cortical systems that process language, as revealed by non-native speech sound perception , 2011, Neuroreport.

[15]  Joy Hirsch,et al.  Distinct cortical areas associated with native and second languages , 1997, Nature.

[16]  D. Boas,et al.  HomER: a review of time-series analysis methods for near-infrared spectroscopy of the brain. , 2009, Applied optics.

[17]  Simone Cutini,et al.  Functional near Infrared Optical Imaging in Cognitive Neuroscience: An Introductory Review , 2012 .

[18]  L. Petitto,et al.  Exploring Cognitive Functions in Babies, Children & Adults with Near Infrared Spectroscopy. , 2009, Journal of visualized experiments : JoVE.

[19]  Trevor B. Penney,et al.  Applications of Near Infrared Spectroscopy and Imaging for Motor Rehabilitation in Stroke Patients , 2009 .

[20]  Joanna A. Christodoulou,et al.  Brain basis of phonological awareness for spoken language in children and its disruption in dyslexia. , 2012, Cerebral cortex.

[21]  P R Kileny,et al.  Cognitive evoked potentials to speech and tonal stimuli in children with implants. , 1997, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[22]  Alan C. Evans,et al.  Speech-like cerebral activity in profoundly deaf people processing signed languages: implications for the neural basis of human language. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Beauchamp,et al.  Neuroimaging with near-infrared spectroscopy demonstrates speech-evoked activity in the auditory cortex of deaf children following cochlear implantation , 2010, Hearing Research.

[24]  Emily B. Myers,et al.  Inferior Frontal Regions Underlie the Perception of Phonetic Category Invariance , 2009, Psychological science.

[25]  David P. Corina,et al.  fMRI auditory language differences between dyslexic and able reading children , 2001, Neuroreport.

[26]  Andreas Büchner,et al.  Residual Neural Processing of Musical Sound Features in Adult Cochlear Implant Users , 2014, Front. Hum. Neurosci..

[27]  Nadine Gaab,et al.  Functional characteristics of developmental dyslexia in left-hemispheric posterior brain regions predate reading onset , 2012, Proceedings of the National Academy of Sciences.

[28]  M. Ferrari,et al.  A brief review on the use of functional near-infrared spectroscopy (fNIRS) for language imaging studies in human newborns and adults , 2012, Brain and Language.

[29]  Yoko Hoshi,et al.  Functional near-infrared spectroscopy: current status and future prospects. , 2007, Journal of biomedical optics.

[30]  L. Petitto,et al.  Bilingual signed and spoken language acquisition from birth: implications for the mechanisms underlying early bilingual language acquisition , 2001, Journal of Child Language.

[31]  M. Dorman,et al.  Minimization of cochlear implant stimulus artifact in cortical auditory evoked potentials , 2006, Clinical Neurophysiology.

[32]  H. Neville,et al.  Maturational Constraints on Functional Specializations for Language Processing: ERP and Behavioral Evidence in Bilingual Speakers , 1996, Journal of Cognitive Neuroscience.

[33]  David Poeppel,et al.  Towards a New Neurobiology of Language , 2012, The Journal of Neuroscience.

[34]  David A. Boas,et al.  Motion artifacts in functional near-infrared spectroscopy: A comparison of motion correction techniques applied to real cognitive data , 2014, NeuroImage.

[35]  Trevor Penney,et al.  Applications of Near Infrared Spectroscopy and Imaging for Motor Rehabilitation in Stroke Patients , 2009 .

[36]  B. Shaywitz,et al.  Dyslexia (Specific Reading Disability) , 2005, Biological Psychiatry.

[37]  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.

[38]  M Wolf,et al.  How to detect and reduce movement artifacts in near-infrared imaging using moving standard deviation and spline interpolation , 2010, Physiological measurement.

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

[40]  Joanna A. Christodoulou,et al.  A meta-analysis of functional reading systems in typically developing and struggling readers across different alphabetic languages , 2015, Front. Psychol..

[41]  Peter A. Bandettini,et al.  Twenty years of functional MRI: The science and the stories , 2012, NeuroImage.

[42]  Steven Pinker,et al.  The biological basis of language: insight from developmental grammatical impairments , 2014, Trends in Cognitive Sciences.

[43]  L. Verhoeven,et al.  Aberrant N400 responses to phonological overlap during rhyme judgements in children at risk for dyslexia , 2013, Brain Research.

[44]  Kenneth Hugdahl,et al.  FMRI brain activation in a finnish family with specific language impairment compared with a normal control group. , 2004, Journal of speech, language, and hearing research : JSLHR.

[45]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[46]  Kuniyoshi L Sakai,et al.  Sign and speech: amodal commonality in left hemisphere dominance for comprehension of sentences. , 2005, Brain : a journal of neurology.

[47]  Y. Yonekura,et al.  Sound-induced activation of auditory cortices in cochlear implant users with post- and prelingual deafness demonstrated by positron emission tomography. , 1997, Acta oto-laryngologica.

[48]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[49]  Keum-Shik Hong,et al.  Kalman estimator- and general linear model-based on-line brain activation mapping by near-infrared spectroscopy , 2010, Biomedical engineering online.

[50]  A. Snik,et al.  Speech-evoked cortical potentials recognition in cochlear implant users and speech , 2001, Scandinavian audiology.

[51]  Angela D. Friederici,et al.  Auditory Language Comprehension in Children with Developmental Dyslexia: Evidence from Event-related Brain Potentials , 2006, Journal of Cognitive Neuroscience.

[52]  Auditory Evoked Potentials under Active and Passive Hearing Conditions in Adult Cochlear Implant Users , 2012, Clinical and experimental otorhinolaryngology.

[53]  P. Julyan,et al.  Auditory cortical activation and speech perception in cochlear implant users , 2007, The Journal of Laryngology & Otology.

[54]  Sophie K. Scott,et al.  Auditory neuroimaging with fMRI and PET , 2014, Hearing Research.

[55]  A. Liberman,et al.  The Angular Gyrus in Developmental Dyslexia: Task-Specific Differences in Functional Connectivity Within Posterior Cortex , 2000, Psychological science.

[56]  E. Grigorenko,et al.  In Search of the Perfect Phenotype: An Analysis of Linkage and Association Studies of Reading and Reading-Related Processes , 2011, Behavior genetics.

[57]  J. Ziegler,et al.  Reading acquisition, developmental dyslexia, and skilled reading across languages: a psycholinguistic grain size theory. , 2005, Psychological bulletin.

[58]  R. Frackowiak,et al.  Differential recruitment of the speech processing system in healthy subjects and rehabilitated cochlear implant patients. , 2000, Brain : a journal of neurology.

[59]  M. Marschark,et al.  Effects of cochlear implants on children's reading and academic achievement. , 2007, Journal of deaf studies and deaf education.

[60]  P. Skudlarski,et al.  Development of left occipitotemporal systems for skilled reading in children after a phonologically- based intervention , 2004, Biological Psychiatry.

[61]  William Winn,et al.  Functional MRI activation in children with and without dyslexia during pseudoword aural repeat and visual decode: before and after treatment. , 2007, Neuropsychology.

[62]  J. Henry,et al.  A meta-analytic review of verbal fluency performance in patients with traumatic brain injury. , 2004, Neuropsychology.

[63]  U. Goswami,et al.  Orthographic influences, vocabulary development, and phonological awareness in deaf children who use cochlear implants , 2009, Applied Psycholinguistics.

[64]  R. Turner,et al.  Characterizing Evoked Hemodynamics with fMRI , 1995, NeuroImage.

[65]  Study of Phonological Awareness of Preschool and School Aged Children with Cochlear Implant and Normal Hearing , 2014, Korean journal of audiology.

[66]  Helmut Remschmidt,et al.  Auditory processing and dyslexia: evidence for a specific speech processing deficit , 1998, Neuroreport.

[67]  Allen R. Braun,et al.  Auditory Cortical Activity During Cochlear Implant-Mediated Perception of Spoken Language, Melody, and Rhythm , 2010, Journal of the Association for Research in Otolaryngology.

[68]  D. Bishop,et al.  Developmental dyslexia and specific language impairment: same or different? , 2004, Psychological bulletin.

[69]  R. Miyamoto,et al.  Positron emission tomography in cochlear implant and auditory brainstem implant recipients. , 2001, Journal of communication disorders.

[70]  P. Tallal.  Improving language and literacy is a matter of time , 2004, Nature Reviews Neuroscience.

[71]  Jack M Fletcher,et al.  Brain Activation Profiles During the Early Stages of Reading Acquisition , 2002, Journal of child 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.