Left premotor cortex and allophonic speech perception in dyslexia: A PET study

Disorders of categorical perception has been put forward as a new account of phonological deficit in dyslexia (Serniclaes, W., Sprenger-Charolles, L., Carre, R. and Demonet, J.F., 2001. Perceptual discrimination of speech sounds in developmental dyslexia. J. Speech Lang. Hear. Res. 44, 384-399.) so that dyslexic subjects tend to discriminate phoneme instances within a given phonemic category rather than between categories, possibly witnessing the persistence of phonemic boundaries of 'allophones' that may be relevant to other languages although not to one's mother tongue (Serniclaes, W., Van Heghe, S., Mousty, P., Carre, R. and Sprenger-Charolles, L., 2004. Allophonic mode of speech perception in dyslexia. J. Exp. Child Psychol. 87, 336-361.). The brain correlates of within- and between-category discrimination were explored using a /ba/-/da/ phonetic continuum and H(2)(15)O PET in 14 dyslexic and 16 control adult readers; subjects discriminated a set of stimuli pairs, first in a 'naïve' (acoustic) condition and, after debriefing about the stimuli identity, in a speech (phonemic) condition (Dufor, O., Serniclaes, W., Sprenger-Charolles, L. and Demonet, J.F., 2007. Top-down processes during auditory phoneme categorization in dyslexia: a PET study. NeuroImage 34, 1692-1707.). While discrimination of 'between' pairs improved in all subjects following debriefing, 'within' stimuli yielded variable performance; some subjects kept discriminating them, while best categorizers judged them identical. Correlation analyses between acoustic-to-speech changes in brain activity and in 'within'-pair discrimination, and between control and dyslexic groups, revealed a criss-crossed correlation pattern in the left BA6 so that the higher the activity the better the categorization in control subjects whereas the higher the activity the more increased 'within' discrimination in dyslexic subjects. Therefore, in average readers, enhanced activity in the left BA6 likely contributes to optimizing phoneme categorization via refined speech motor coding. In dyslexic subjects showing sensitivity to 'within'-category cues, activity enhancement in this region might suggest the persistence of motor coding for allophonic representations of speech.

[1]  J. Brandt,et al.  Auditory phonemic perception in dyslexia: Categorical identification and discrimination of stop consonants , 1980, Brain and Language.

[2]  Karl J. Friston,et al.  A PET study of word finding , 1991, Neuropsychologia.

[3]  B. Vogt,et al.  Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex , 1998, Experimental Brain Research.

[4]  P. Tallal,et al.  Defects of Non-Verbal Auditory Perception in Children with Developmental Aphasia , 1973, Nature.

[5]  B. J. Casey,et al.  Regional brain activity when selecting a response despite interference: An H2 15O PET study of the stroop and an emotional stroop , 1994, Human brain mapping.

[6]  Richard S. J. Frackowiak,et al.  Brain activity during reading. The effects of exposure duration and task. , 1994, Brain : a journal of neurology.

[7]  Christophe Pallier,et al.  Anatomical correlates of foreign speech sound production. , 2006, Cerebral cortex.

[8]  Karl J. Friston,et al.  Investigations of the functional anatomy of attention using the stroop test , 1993, Neuropsychologia.

[9]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

[10]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[11]  F Fazio,et al.  Brain abnormalities underlying altered activation in dyslexia: a voxel based morphometry study. , 2005, Brain : a journal of neurology.

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

[13]  Hiroshi Fukuda,et al.  Functional anatomy of GO/NO-GO discrimination and response selection — a PET study in man , 1996, Brain Research.

[14]  J. Stein,et al.  To see but not to read; the magnocellular theory of dyslexia , 1997, Trends in Neurosciences.

[15]  M. Sigman,et al.  Functional organization of perisylvian activation during presentation of sentences in preverbal infants , 2006, Proceedings of the National Academy of Sciences.

[16]  Jeffrey R. Binder,et al.  Left Posterior Temporal Regions are Sensitive to Auditory Categorization , 2008, Journal of Cognitive Neuroscience.

[17]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. II. Subcortical structures and learning by trial and error. , 1997, Journal of neurophysiology.

[18]  Alan C. Evans,et al.  Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. , 1993, Journal of neurophysiology.

[19]  A. Hillis,et al.  Re-examining the brain regions crucial for orchestrating speech articulation. , 2004, Brain : a journal of neurology.

[20]  C. Liégeois-Chauvel,et al.  Asymmetry of voice onset time-processing in adult developmental dyslexics , 2008, Clinical Neurophysiology.

[21]  J. Werker,et al.  Phonemic and phonetic factors in adult cross-language speech perception. , 1984, The Journal of the Acoustical Society of America.

[22]  Ioana Chitoran,et al.  Approaches to phonological complexity , 2009 .

[23]  P. Kuhl,et al.  Cross-language analysis of phonetic units in language addressed to infants. , 1997, Science.

[24]  S. Borgwaldt Reading acquisition and developmental dyslexia , 2010 .

[25]  J. Démonet,et al.  Perceptual discrimination of speech sounds in developmental dyslexia. , 2001, Journal of speech, language, and hearing research : JSLHR.

[26]  Serge Ruff,et al.  Neural substrates of impaired categorical perception of phonemes in adult dyslexics: An fMRI study , 2003, Brain and Cognition.

[27]  Jean-François Démonet,et al.  Top-down processes during auditory phoneme categorization in dyslexia: A PET study , 2007, NeuroImage.

[28]  E. Phelps,et al.  FMRI of the prefrontal cortex during overt verbal fluency , 1997, Neuroreport.

[29]  Stuart Rosen,et al.  Auditory processing in dyslexia and specific language impairment: is there a deficit? What is its nature? Does it explain anything? , 2003, J. Phonetics.

[30]  Robert J Zatorre,et al.  Learning new sounds of speech: reallocation of neural substrates , 2004, NeuroImage.

[31]  Willy Serniclaes,et al.  Neural correlates of switching from auditory to speech perception , 2005, NeuroImage.

[32]  David A. Medler,et al.  Cerebral Cortex doi:10.1093/cercor/bhi040 Cerebral Cortex Advance Access published February 9, 2005 , 2022 .

[33]  D. Burnham Language specific speech perception and the onset of reading , 2003 .

[34]  Karl J. Friston,et al.  Exploring the temporal nature of hemodynamic responses of cortical motor areas using functional MRI , 1998, Neurology.

[35]  T. Braver,et al.  Anterior Cingulate Cortex and Response Conflict : Effects of Response Modality and Processing Domain , 2022 .

[36]  John Jonides,et al.  Dissociable neural mechanisms underlying response-based and familiarity-based conflict in working memory , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[37]  E. Paulesu,et al.  When all hypotheses are right: A multifocal account of dyslexia , 2009, Human brain mapping.

[38]  N. Dronkers A new brain region for coordinating speech articulation , 1996, Nature.

[39]  B. C. Griffith,et al.  The discrimination of speech sounds within and across phoneme boundaries. , 1957, Journal of experimental psychology.

[40]  J. Démonet The dynamics of language-related brain images , 2005, Neurocase.

[41]  B. Horwitz,et al.  Functional connectivity of the angular gyrus in normal reading and dyslexia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[43]  T. Braver,et al.  Anterior cingulate cortex and response conflict: effects of response modality and processing domain. , 2001, Cerebral Cortex.

[44]  K. Botteron,et al.  Is attention-deficit/hyperactivity disorder an energy deficiency syndrome? , 2001, Biological Psychiatry.

[45]  J. Millichap,et al.  Brain Activity During Reading , 1995 .

[46]  F. Fazio,et al.  Dyslexia: Cultural Diversity and Biological Unity , 2001, Science.

[47]  P. Marquis,et al.  Auditory evoked potential patterns to voiced and voiceless speech sounds in adult developmental dyslexics with persistent deficits. , 2005, Cerebral cortex.

[48]  Lucie Hertz-Pannier,et al.  Nature and nurture in language acquisition: anatomical and functional brain-imaging studies in infants , 2006, Trends in Neurosciences.

[49]  C Büchel,et al.  Brain regions involved in articulation , 1999, The Lancet.

[50]  David A. Medler,et al.  Neural correlates of sensory and decision processes in auditory object identification , 2004, Nature Neuroscience.

[51]  G. Thierry,et al.  Renewal of the neurophysiology of language: functional neuroimaging. , 2005, Physiological reviews.

[52]  F. Ramus,et al.  Theories of developmental dyslexia: insights from a multiple case study of dyslexic adults. , 2003, Brain : a journal of neurology.

[53]  L. Sprenger-Charolles,et al.  Discrimination of speech sounds by children with dyslexia: comparisons with chronological age and reading level controls. , 2008, Journal of experimental child psychology.

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

[55]  Emily B. Myers,et al.  An event-related fMRI investigation of voice-onset time discrimination , 2008, NeuroImage.

[56]  L. Sprenger-Charolles,et al.  Allophonic mode of speech perception in dyslexia. , 2004, Journal of experimental child psychology.

[57]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[58]  Serge Ruff,et al.  Enhanced response of the left frontal cortex to slowed down speech in dyslexia: an fMRI study , 2002, Neuroreport.

[59]  Emily B. Myers,et al.  The Perception of Voice Onset Time: An fMRI Investigation of Phonetic Category Structure , 2005, Journal of Cognitive Neuroscience.

[60]  K. Kiehl,et al.  Neural sources involved in auditory target detection and novelty processing: an event-related fMRI study. , 2001, Psychophysiology.