Speech-induced suppression of evoked auditory fields in children who stutter

Auditory responses to speech sounds that are self-initiated are suppressed compared to responses to the same speech sounds during passive listening. This phenomenon is referred to as speech-induced suppression, a potentially important feedback-mediated speech-motor control process. In an earlier study, we found that both adults who do and do not stutter demonstrated a reduced amplitude of the auditory M50 and M100 responses to speech during active production relative to passive listening. It is unknown if auditory responses to self-initiated speech-motor acts are suppressed in children or if the phenomenon differs between children who do and do not stutter. As stuttering is a developmental speech disorder, examining speech-induced suppression in children may identify possible neural differences underlying stuttering close to its time of onset. We used magnetoencephalography to determine the presence of speech-induced suppression in children and to characterize the properties of speech-induced suppression in children who stutter. We examined the auditory M50 as this was the earliest robust response reproducible across our child participants and the most likely to reflect a motor-to-auditory relation. Both children who do and do not stutter demonstrated speech-induced suppression of the auditory M50. However, children who stutter had a delayed auditory M50 peak latency to vowel sounds compared to children who do not stutter indicating a possible deficiency in their ability to efficiently integrate auditory speech information for the purpose of establishing neural representations of speech sounds.

[1]  Nancy J Cox,et al.  Genomewide significant linkage to stuttering on chromosome 12. , 2005, American journal of human genetics.

[2]  K M Heilman,et al.  Anomalous anatomy of speech–language areas in adults with persistent developmental stuttering , 2001, Neurology.

[3]  S. Kapur,et al.  A positron emission tomography study of silent and oral single word reading in stuttering and nonstuttering adults. , 2000, Journal of speech, language, and hearing research : JSLHR.

[4]  Carles Escera,et al.  Abnormal speech sound representation in persistent developmental stuttering , 2005, Neurology.

[5]  Mark A. Hasegawa-Johnson,et al.  Brain anatomy differences in childhood stuttering , 2008, NeuroImage.

[6]  B. Garreau,et al.  Neuroimaging in child neuropsychiatric disorders , 1998, Springer Berlin Heidelberg.

[7]  Xiaojuan Guo,et al.  [Gray matter abnormalities in developmental stuttering determined with voxel-based morphometry]. , 2007, Zhonghua yi xue za zhi.

[8]  M. Merzenich,et al.  Modulation of the Auditory Cortex during Speech: An MEG Study , 2002, Journal of Cognitive Neuroscience.

[9]  D. Burnham,et al.  The delayed trigger voice key: An improved analogue voice key for psycholinguistic research , 2005, Behavior research methods.

[10]  R. Ingham,et al.  Brain correlates of stuttering and syllable production. A PET performance-correlation analysis. , 2000 .

[11]  N J Cox,et al.  The genetic basis of persistence and recovery in stuttering. , 1997, Journal of speech, language, and hearing research : JSLHR.

[12]  V. Gracco,et al.  Perceptual recalibration of speech sounds following speech motor learning. , 2009, The Journal of the Acoustical Society of America.

[13]  G Weismer,et al.  Interspeaker variation in habitual speaking rate: evidence for a neuromuscular component. , 1997, Journal of speech, language, and hearing research : JSLHR.

[14]  Margot J. Taylor,et al.  Electrophysiological Evaluation of Human Brain Development , 2007, Developmental neuropsychology.

[15]  K. Watkins,et al.  Structural and functional abnormalities of the motor system in developmental stuttering. , 2007, Brain : a journal of neurology.

[16]  P. Howie,et al.  Concordance for stuttering in monozygotic and dizygotic twin pairs. , 1981, Journal of speech and hearing research.

[17]  Vincent L. Gracco,et al.  The effects of simulated stuttering and prolonged speech on the neural activation patterns of stuttering and nonstuttering adults , 2008, Brain and Language.

[18]  O. Bloodstein,et al.  Some empirical observations about early stuttering: a possible link to language development. , 2006, Journal of communication disorders.

[19]  Kensuke Sekihara,et al.  Modified beamformers for coherent source region suppression , 2006, IEEE Transactions on Biomedical Engineering.

[20]  C. Büchel,et al.  Disconnection of speech-relevant brain areas in persistent developmental stuttering , 2022 .

[21]  E. Charles Healey,et al.  Stuttering severity instrument for children and adults , 1991 .

[22]  Nancy J Cox,et al.  New complexities in the genetics of stuttering: significant sex-specific linkage signals. , 2006, American journal of human genetics.

[23]  Abraham Z. Snyder,et al.  The Feasibility of a Common Stereotactic Space for Children and Adults in fMRI Studies of Development , 2002, NeuroImage.

[24]  Christine Preibisch,et al.  The nature and treatment of stuttering as revealed by fMRI A within- and between-group comparison. , 2003, Journal of fluency disorders.

[25]  Gareth R. Barnes,et al.  Group imaging of task-related changes in cortical synchronisation using nonparametric permutation testing , 2003, NeuroImage.

[26]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[27]  R Hari,et al.  Evidence for cortical origin of the 40 Hz auditory evoked response in man. , 1987, Electroencephalography and clinical neurophysiology.

[28]  John O. Willis,et al.  Peabody Picture Vocabulary Test–Third Edition , 2008 .

[29]  G. Curio,et al.  Speaking modifies voice‐evoked activity in the human auditory cortex , 2000, Human brain mapping.

[30]  Carole Ober,et al.  Genetic studies of stuttering in a founder population. , 2007, Journal of fluency disorders.

[31]  S. Nagarajan,et al.  Speech target modulates speaking induced suppression in auditory cortex , 2009, BMC Neuroscience.

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

[33]  C. Ludlow,et al.  Stuttering: a dynamic motor control disorder. , 2003, Journal of fluency disorders.

[34]  O. Salonen,et al.  Auditory Evoked Magnetic Fields to Tones and Pseudowords in Healthy Children and Adults , 1995, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[35]  H. Fukuyama,et al.  Cortical processing mechanism for vocalization with auditory verbal feedback , 1997, Neuroreport.

[36]  Frank H. Guenther,et al.  Unstable or Insufficiently Activated Internal Models and Feedback-Biased Motor Control as Sources of Dysfluency: A Theoretical Model of Stuttering , 2004 .

[37]  E. Darcy Burgund,et al.  Comparison of functional activation foci in children and adults using a common stereotactic space , 2003, NeuroImage.

[38]  Riitta Salmelin,et al.  Subject's own speech reduces reactivity of the human auditory cortex , 1999, Neuroscience Letters.

[39]  Vincent L. Gracco,et al.  Auditory evoked fields to vocalization during passive listening and active generation in adults who stutter , 2010, NeuroImage.

[40]  Donald E. Mowrer,et al.  Stuttering severity instrument for children and adults , 1991 .

[41]  David Poeppel,et al.  Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique , 2001, IEEE Transactions on Biomedical Engineering.

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

[43]  D. Cheyne,et al.  Spatiotemporal mapping of cortical activity accompanying voluntary movements using an event‐related beamforming approach , 2006, Human brain mapping.

[44]  Timothy P L Roberts,et al.  Cortical auditory system maturational abnormalities in children with autism disorder: an MEG investigation. , 2003, Brain research. Developmental brain research.

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

[46]  Lori L. Holt,et al.  Reflections on mirror neurons and speech perception , 2009, Trends in Cognitive Sciences.

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

[48]  W. Roberts,et al.  Prominence of M50 auditory evoked response over M100 in childhood and autism , 2004, Neuroreport.

[49]  Rebecca Treiman,et al.  Phonetic Biases in Voice Key Response Time Measurements , 2002 .

[50]  Christine Preibisch,et al.  Cortical plasticity associated with stuttering therapy. , 2005, Journal of fluency disorders.

[51]  Raymond D. Kent,et al.  An auditory-feedback-based neural network model of speech production that is robust to developmental changes in the size and shape of the articulatory system. , 2000, Journal of speech, language, and hearing research : JSLHR.

[52]  O. Muzik,et al.  Statistical Parametric Mapping: Assessment of Application in Children , 2000, NeuroImage.

[53]  T. Yoshimoto,et al.  Middle and long latency peak sources in auditory evoked magnetic fields for tone bursts in humans , 2000, Neuroscience Letters.

[54]  Riitta Salmelin,et al.  Right rolandic activation during speech perception in stutterers: a MEG study , 2005, NeuroImage.

[55]  Christine Weber-Fox,et al.  Atypical neural functions underlying phonological processing and silent rehearsal in children who stutter. , 2008, Developmental science.

[56]  K M Heilman,et al.  Aberrant auditory processing and atypical planum temporale in developmental stuttering , 2004, Neurology.

[57]  S. Nagarajan,et al.  Magnetoencephalographic evidence for a precise forward model in speech production , 2006, Neuroreport.

[58]  Srikantan S Nagarajan,et al.  Preliminary results of a functional MRI study of brain activation patterns in stuttering and nonstuttering speakers during a lexical access task. , 2003, Journal of fluency disorders.

[59]  R E Carson,et al.  Altered patterns of cerebral activity during speech and language production in developmental stuttering. An H2(15)O positron emission tomography study. , 1997, Brain : a journal of neurology.

[60]  Frank H. Guenther,et al.  Learning Sound Categories: A Neural Model and Supporting Experiments , 2002 .

[61]  Youxin Wang,et al.  Association between dopaminergic genes (SLC6A3 and DRD2) and stuttering among Han Chinese , 2009, Journal of Human Genetics.

[62]  Christine Weber-Fox,et al.  Non-linguistic auditory processing in stuttering: evidence from behavior and event-related brain potentials. , 2008, Journal of fluency disorders.

[63]  D. Poeppel,et al.  Latency of the auditory evoked neuromagnetic field components: stimulus dependence and insights toward perception. , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[64]  J. Eggermont,et al.  Auditory Evoked Potentials: Basic Principles and Clinical Application , 2006 .

[65]  P. Teale,et al.  Developmental changes in refractoriness of the neuromagnetic M100 in children , 1998, Neuroreport.

[66]  E. Yairi,et al.  Early childhood stuttering I: persistency and recovery rates. , 1999, Journal of speech, language, and hearing research : JSLHR.

[67]  R. Kotecha,et al.  Modeling the Developmental Patterns of Auditory Evoked Magnetic Fields in Children , 2009, PloS one.

[68]  F. Guenther Cortical interactions underlying the production of speech sounds. , 2006, Journal of communication disorders.

[69]  N. Bruneau,et al.  Auditory evoked potentials (N1 wave) as indices of cortical development , 1998 .

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

[71]  Willem J. M. Levelt,et al.  Speech, gesture and the origins of language , 2004, European Review.

[72]  Peter D. Neilson,et al.  Speech motor control and stuttering: A computational model of adaptive sensory-motor processing , 1987, Speech Commun..

[73]  Douglas O. Cheyne,et al.  Reconstruction of correlated brain activity with adaptive spatial filters in MEG , 2010, NeuroImage.

[74]  Luc F De Nil,et al.  Voxel-based morphometry of auditory and speech-related cortex in stutterers , 2007, Neuroreport.

[75]  Pascal Perrier,et al.  A theory of speech motor control and supporting data from speakers with normal hearing and with profound hearing loss , 2000, J. Phonetics.

[76]  Soo-Eun Chang,et al.  Brain activation abnormalities during speech and non-speech in stuttering speakers , 2009, NeuroImage.

[77]  Bernd J. Kröger,et al.  Towards a neurocomputational model of speech production and perception , 2009, Speech Commun..

[78]  J. Mäkelä,et al.  Neuromagnetic responses of the human auditory cortex to on- and offsets of noise bursts. , 1987, Audiology : official organ of the International Society of Audiology.

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

[80]  Sylvain Houle,et al.  Functional neuroimaging of cerebellar activation during single word reading and verb generation in stuttering and nonstuttering adults , 2001, Neuroscience Letters.

[81]  James C Mullikin,et al.  Mutations in the lysosomal enzyme-targeting pathway and persistent stuttering. , 2010, The New England journal of medicine.

[82]  R. Ingham,et al.  A PET study of the neural systems of stuttering , 1996, Nature.

[83]  Jason A. Tourville,et al.  Neural mechanisms underlying auditory feedback control of speech , 2008, NeuroImage.

[84]  C. Lu,et al.  The role of large-scale neural interactions for developmental stuttering , 2009, Neuroscience.

[85]  Wilkin Chau,et al.  Determination of activation areas in the human auditory cortex by means of synthetic aperture magnetometry , 2003, NeuroImage.

[86]  Elizabeth W. Pang,et al.  Event-related beamforming: A robust method for presurgical functional mapping using MEG , 2007, Clinical Neurophysiology.

[87]  R. Ingham,et al.  Stuttered and fluent speech production: An ALE meta‐analysis of functional neuroimaging studies , 2005, Human brain mapping.

[88]  Lutz Jäncke,et al.  Morphological brain differences between adult stutterers and non-stutterers , 2004, BMC neurology.

[89]  A. Giraud,et al.  Severity of dysfluency correlates with basal ganglia activity in persistent developmental stuttering , 2008, Brain and Language.

[90]  F. Guenther,et al.  Overreliance on auditory feedback may lead to sound/syllable repetitions: simulations of stuttering and fluency-inducing conditions with a neural model of speech production. , 2010, Journal of fluency disorders.

[91]  Gérard Bailly,et al.  Learning to speak. Sensori-motor control of speech movements , 1997, Speech Commun..

[92]  Frank H. Guenther,et al.  A neural theory of speech acquisition and production , 2012, Journal of Neurolinguistics.

[93]  K K Kidd,et al.  Vertical transmission of susceptibility to stuttering with sex-modified expression. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[94]  O. Bloodstein A handbook on stuttering , 1969 .