Neural entrainment to rhythmic speech in children with developmental dyslexia

A rhythmic paradigm based on repetition of the syllable “ba” was used to study auditory, visual, and audio-visual oscillatory entrainment to speech in children with and without dyslexia using EEG. Children pressed a button whenever they identified a delay in the isochronous stimulus delivery (500 ms; 2 Hz delta band rate). Response power, strength of entrainment and preferred phase of entrainment in the delta and theta frequency bands were compared between groups. The quality of stimulus representation was also measured using cross-correlation of the stimulus envelope with the neural response. The data showed a significant group difference in the preferred phase of entrainment in the delta band in response to the auditory and audio-visual stimulus streams. A different preferred phase has significant implications for the quality of speech information that is encoded neurally, as it implies enhanced neuronal processing (phase alignment) at less informative temporal points in the incoming signal. Consistent with this possibility, the cross-correlogram analysis revealed superior stimulus representation by the control children, who showed a trend for larger peak r-values and significantly later lags in peak r-values compared to participants with dyslexia. Significant relationships between both peak r-values and peak lags were found with behavioral measures of reading. The data indicate that the auditory temporal reference frame for speech processing is atypical in developmental dyslexia, with low frequency (delta) oscillations entraining to a different phase of the rhythmic syllabic input. This would affect the quality of encoding of speech, and could underlie the cognitive impairments in phonological representation that are the behavioral hallmark of this developmental disorder across languages.

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

[2]  John J. Foxe,et al.  Oscillatory Sensory Selection Mechanisms during Intersensory Attention to Rhythmic Auditory and Visual Inputs: A Human Electrocorticographic Investigation , 2011, The Journal of Neuroscience.

[3]  A. Rees,et al.  Sensitivity to dynamic auditory and visual stimuli predicts nonword reading ability in both dyslexic and normal readers , 1998, Current Biology.

[4]  Victoria Leong,et al.  Impaired perception of syllable stress in children with dyslexia: A longitudinal study , 2013 .

[5]  Jan Wouters,et al.  Auditory Steady State Cortical Responses Indicate Deviant Phonemic-Rate Processing in Adults With Dyslexia , 2012, Ear and hearing.

[6]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[7]  Usha Goswami,et al.  Neural Entrainment to Rhythmically Presented Auditory, Visual, and Audio-Visual Speech in Children , 2012, Front. Psychology.

[8]  Ramesh Srinivasan,et al.  Suppression of competing speech through entrainment of cortical oscillations. , 2013, Journal of neurophysiology.

[9]  Jarmo A. Hämäläinen,et al.  Reduced phase locking to slow amplitude modulation in adults with dyslexia: An MEG study , 2012, NeuroImage.

[10]  James R. Brockmole,et al.  History of Reading Struggles Linked to Enhanced Learning in Low Spatial Frequency Scenes , 2012, PloS one.

[11]  D. Poeppel,et al.  Phase Patterns of Neuronal Responses Reliably Discriminate Speech in Human Auditory Cortex , 2007, Neuron.

[12]  D. Poeppel,et al.  Auditory Cortex Tracks Both Auditory and Visual Stimulus Dynamics Using Low-Frequency Neuronal Phase Modulation , 2010, PLoS biology.

[13]  K. Eklund,et al.  Developmental Pathways of Children With and Without Familial Risk for Dyslexia During the First Years of Life , 2001, Developmental neuropsychology.

[14]  E. Marinus,et al.  Australian comparison data for the Test of Word Reading Efficiency (TOWRE) , 2013 .

[15]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.

[16]  S. Donnadieu,et al.  Auditory and visual stream segregation in children and adults: An assessment of the amodality assumption of the ‘sluggish attentional shifting’ theory of dyslexia , 2009, Brain Research.

[17]  John J. Foxe,et al.  At what time is the cocktail party? A late locus of selective attention to natural speech , 2012, The European journal of neuroscience.

[18]  Benedict Shien Wei Ng,et al.  EEG phase patterns reflect the selectivity of neural firing. , 2013, Cerebral cortex.

[19]  Paavo H. T. Leppänen,et al.  Basic Auditory Processing Deficits in Dyslexia , 2013, Journal of learning disabilities.

[20]  Franck Ramus,et al.  Altered Low-Gamma Sampling in Auditory Cortex Accounts for the Three Main Facets of Dyslexia , 2011, Neuron.

[21]  Sylviane Valdois,et al.  Sequential Versus Simultaneous Processing Deficits in Developmental Dyslexia , 2012 .

[22]  U. Goswami,et al.  Audiovisual perception of noise vocoded speech in dyslexic and non-dyslexic adults: The role of low-frequency visual modulations , 2013, Brain and Language.

[23]  David Poeppel,et al.  The analysis of speech in different temporal integration windows: cerebral lateralization as 'asymmetric sampling in time' , 2003, Speech Commun..

[24]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[25]  D. Poeppel,et al.  Neural Response Phase Tracks How Listeners Learn New Acoustic Representations , 2013, Current Biology.

[26]  B. Hangya,et al.  Phase Entrainment of Human Delta Oscillations Can Mediate the Effects of Expectation on Reaction Speed , 2010, The Journal of Neuroscience.

[27]  Tim Fosker,et al.  Language-universal Sensory Deficits in Developmental Dyslexia: English, Spanish, and Chinese , 2011, Journal of Cognitive Neuroscience.

[28]  C. Schroeder,et al.  Tuning of the Human Neocortex to the Temporal Dynamics of Attended Events , 2011, The Journal of Neuroscience.

[29]  C. Woolger,et al.  Wechsler Intelligence Scale for Children-Third Edition (wisc-iii) , 2001 .

[30]  D. Poeppel,et al.  Speech Perception from a Neurophysiological Perspective , 2012 .

[31]  U. Goswami,et al.  Assessment of rhythmic entrainment at multiple timescales in dyslexia: Evidence for disruption to syllable timing , 2014, Hearing Research.

[32]  U. Goswami A temporal sampling framework for developmental dyslexia , 2011, Trends in Cognitive Sciences.

[33]  Steven Greenberg,et al.  Temporal properties of spontaneous speech - a syllable-centric perspective , 2003, J. Phonetics.

[34]  Victoria Leong,et al.  Differential Entrainment of Neuroelectric Delta Oscillations in Developmental Dyslexia , 2013, PloS one.

[35]  Usha Goswami,et al.  Auditory and motor rhythm awareness in adults with dyslexia , 2006 .

[36]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[37]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

[38]  U. Goswami,et al.  Rhythmic processing in children with developmental dyslexia: Auditory and motor rhythms link to reading and spelling , 2008, Journal of Physiology-Paris.

[39]  A. Puce,et al.  Neuronal oscillations and visual amplification of speech , 2008, Trends in Cognitive Sciences.

[40]  Susan E. Stothard,et al.  Is preschool language impairment a risk factor for dyslexia in adolescence? , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[41]  D. Abrams,et al.  Abnormal Cortical Processing of the Syllable Rate of Speech in Poor Readers , 2009, The Journal of Neuroscience.

[42]  G. Kanji,et al.  The development of analysis of variance for circular data , 1988 .

[43]  J. McClellan,et al.  Chebyshev Approximation for Nonrecursive Digital Filters with Linear Phase , 1972 .

[44]  M. Zorzi,et al.  Visual spatial attention and speech segmentation are both impaired in preschoolers at familial risk for developmental dyslexia. , 2010, Dyslexia.

[45]  F. Ramus,et al.  What Phonological Deficit? , 2008, Quarterly journal of experimental psychology.

[46]  Steven Greenberg,et al.  On the Possible Role of Brain Rhythms in Speech Perception: Intelligibility of Time-Compressed Speech with Periodic and Aperiodic Insertions of Silence , 2009, Phonetica.

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