Electrophysiological correlates of impaired reading in dyslexic pre-adolescent children

In this study, event related potentials (ERPs) were used to investigate the extent to which dyslexics (aged 9-13 years) differ from normally reading controls in early ERPs, which reflect prelexical orthographic processing, and in late ERPs, which reflect implicit phonological processing. The participants performed an implicit reading task, which was manipulated in terms of letter-specific processing, orthographic familiarity, and phonological structure. Comparing consonant- and symbol sequences, the results showed significant differences in the P1 and N1 waveforms in the control but not in the dyslexic group. The reduced P1 and N1 effects in pre-adolescent children with dyslexia suggest a lack of visual specialization for letter-processing. The P1 and N1 components were not sensitive to the familiar vs. less familiar orthographic sequence contrast. The amplitude of the later N320 component was larger for phonologically legal (pseudowords) compared to illegal (consonant sequences) items in both controls and dyslexics. However, the topographic differences showed that the controls were more left-lateralized than the dyslexics. We suggest that the development of the mechanisms that support literacy skills in dyslexics is both delayed and follows a non-normal developmental path. This contributes to the hemispheric differences observed and might reflect a compensatory mechanism in dyslexics.

[1]  J. Maisog,et al.  A positron emission tomographic study of impaired word recognition and phonological processing in dyslexic men. , 1997, Archives of neurology.

[2]  Devin M. Kearns,et al.  The neurobiology of dyslexia , 2001, Clinical Neuroscience Research.

[3]  J. Maisog,et al.  A Meta‐analysis of Functional Neuroimaging Studies of Dyslexia , 2008, Annals of the New York Academy of Sciences.

[4]  P. Holcomb,et al.  Event-Related Brain Potentials Elicited during Phonological Processing Differentiate Subgroups of Reading Disabled Adolescents , 1998, Brain and Language.

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

[6]  B. Shaywitz,et al.  Dyslexia (specific reading disability). , 2003, Pediatrics in review.

[7]  C. Luzzatti,et al.  Do Italian dyslexic children use the lexical reading route efficiently? An orthographic judgment task , 2009 .

[8]  J. Leon Kenemans,et al.  Electrophysiological correlates of cortico-subcortical interaction: A cross-frequency spectral EEG analysis , 2006, Clinical Neurophysiology.

[9]  Grégory Simon,et al.  CHRONOMETRY OF VISUAL WORD RECOGNITION DURING PASSIVE AND LEXICAL DECISION TASKS: AN ERP INVESTIGATION , 2004, The International journal of neuroscience.

[10]  Daniel Brandeis,et al.  Tuning of the visual word processing system: Distinct developmental ERP and fMRI effects , 2009, Human brain mapping.

[11]  Daniel Brandeis,et al.  Emerging Neurophysiological Specialization for Letter Strings , 2005, Journal of Cognitive Neuroscience.

[12]  H Wimmer,et al.  The nonword reading deficit in developmental dyslexia: evidence from children learning to read German. , 1996, Journal of experimental child psychology.

[13]  Bruce D. McCandliss,et al.  The visual word form area: expertise for reading in the fusiform gyrus , 2003, Trends in Cognitive Sciences.

[14]  Zhong-Lin Lu,et al.  Sensitivity to orthographic familiarity in the occipito-temporal region , 2008, NeuroImage.

[15]  W. Kaiser,et al.  fMRI during word processing in dyslexic and normal reading children. , 1999, Neuroreport.

[16]  Daniel Brandeis,et al.  The development of print tuning in children with dyslexia: Evidence from longitudinal ERP data supported by fMRI , 2011, NeuroImage.

[17]  Friedemann Pulvermüller,et al.  Early influences of word length and frequency: a group study using MEG , 2003, Neuroreport.

[18]  R. Dykman,et al.  Visual event-related potentials of dyslexic children to rhyming and nonrhyming stimuli. , 1994, Journal of clinical and experimental neuropsychology.

[19]  J. Ziegler,et al.  Phonological Information Provides Early Sources of Constraint in the Processing of Letter Strings , 1995 .

[20]  Bruce D. McCandliss,et al.  Development of neural systems for reading. , 2007, Annual review of neuroscience.

[21]  H. Wimmer,et al.  A dual-route perspective on poor reading in a regular orthography: Evidence from phonological and orthographic lexical decisions , 2008, Cognitive neuropsychology.

[22]  Joseph K. Torgesen,et al.  Development of Reading-Related Phonological Processing Abilities: New Evidence of Bidirectional Causality from a Latent Variable Longitudinal Study. , 1994 .

[23]  Daniel Brandeis,et al.  Children with dyslexia lack multiple specializations along the visual word-form (VWF) system , 2009, NeuroImage.

[24]  Daniel Brandeis,et al.  Evidence for developmental changes in the visual word processing network beyond adolescence , 2006, NeuroImage.

[25]  Naira A. Taroyan,et al.  Reading words and pseudowords in dyslexia: ERP and behavioural tests in English-speaking adolescents. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[26]  Christian Gaser,et al.  Phonological processing in dyslexic children: a study combining functional imaging and event related potentials , 2002, Neuroscience Letters.

[27]  Michael W. L. Chee,et al.  Frequency of Concrete Words Modulates Prefrontal Activation during Semantic Judgments , 2002, NeuroImage.

[28]  Riitta Salmelin,et al.  Cortical Sequence of Word Perception in Beginning Readers , 2006, The Journal of Neuroscience.

[29]  S. Dehaene Reading in the Brain: The New Science of How We Read , 2009 .

[30]  L. Jancke,et al.  ERP differences of pre-lexical processing between dyslexic and non-dyslexic children. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[31]  J. Pernier,et al.  ERP Manifestations of Processing Printed Words at Different Psycholinguistic Levels: Time Course and Scalp Distribution , 1999, Journal of Cognitive Neuroscience.

[32]  Daniel Brandeis,et al.  Coarse neural tuning for print peaks when children learn to read , 2006, NeuroImage.

[33]  K. Stanovich,et al.  Phenotypic performance profile of children with reading disabilities: A regression-based test of the phonological-core variable-difference model. , 1994 .

[34]  F. Pulvermüller,et al.  Effects of word length and frequency on the human event-related potential , 2004, Clinical Neurophysiology.

[35]  R. Salmelin,et al.  Dynamics of letter string perception in the human occipitotemporal cortex. , 1999, Brain : a journal of neurology.

[36]  Daniel Brandeis,et al.  Impaired tuning of a fast occipito-temporal response for print in dyslexic children learning to read. , 2007, Brain : a journal of neurology.

[37]  S. Dehaene,et al.  Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area. , 2002, Brain : a journal of neurology.

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

[39]  J. Tijms Verbal Memory and Phonological Processing in Dyslexia. , 2004 .

[40]  K. Petersson,et al.  Literacy: a cultural influence on functional left–right differences in the inferior parietal cortex , 2007, The European journal of neuroscience.

[41]  P. Ackerman,et al.  A STUDY OF READING DISABILITY USING EVENT-RELATED BRAIN POTENTIALS ELICITED DURING AUDITORY ALLITERATION JUDGMENTS , 1999 .

[42]  A. Mechelli,et al.  Effect of word and syllable frequency on activation during lexical decision and reading aloud , 2006, Human brain mapping.

[43]  A. Liberman,et al.  Functional disruption in the organization of the brain for reading in dyslexia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[44]  B. Shaywitz,et al.  Paying attention to reading: The neurobiology of reading and dyslexia , 2008, Development and Psychopathology.

[45]  Frank R. Vellutino,et al.  Phonological Coding, Phonological Awareness, and Reading Ability: Evidence from a Longitudinal and Experimental Study. , 1987 .

[46]  Friedemann Pulvermüller,et al.  Modulation of brain activity by multiple lexical and word form variables in visual word recognition: A parametric fMRI study , 2008, NeuroImage.

[47]  R. Salmelin,et al.  Dissociation of normal feature analysis and deficient processing of letter-strings in dyslexic adults. , 1999, Cerebral cortex.

[48]  Sally E. Shaywitz,et al.  Overcoming Dyslexia: A New and Complete Science-Based Program for Reading Problems at Any Level , 2003 .

[49]  A. Mechelli,et al.  Reading and reading disturbance , 2005, Current Opinion in Neurobiology.

[50]  H. Wimmer,et al.  Functional abnormalities in the dyslexic brain: A quantitative meta‐analysis of neuroimaging studies , 2009, Human brain mapping.

[51]  H. Wimmer,et al.  Evidence for a dysfunction of left posterior reading areas in German dyslexic readers , 2006, Neuropsychologia.

[52]  Rebecca Elsaesser,et al.  The sense of smell, its signalling pathways, and the dichotomy of cilia and microvilli in olfactory sensory cells , 2007, BMC Neuroscience.

[53]  P. F. Jong,et al.  Developmental changes in the manifestation of a phonological deficit in dyslexic children learning to read a regular orthography. , 2003 .

[54]  D. Burman,et al.  Deficient orthographic and phonological representations in children with dyslexia revealed by brain activation patterns. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[55]  J. Raven Coloured progressive matrices : sets A, Ab, B , 1956 .

[56]  T. Whitlock Dyslexia , 1989, The Lancet.

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

[58]  M. Posner,et al.  Establishing a time‐line of word recognition: evidence from eye movements and event‐related potentials , 1998, Neuroreport.

[59]  K. Pugh,et al.  The Neurobiological Basis of Skilled and Impaired Reading: Recent Findings and New Directions , 2004, The Cognitive Neuroscience of Reading.

[60]  William D. Marslen-Wilson,et al.  The time course of visual word recognition as revealed by linear regression analysis of ERP data , 2006, NeuroImage.

[61]  H. Wimmer,et al.  A dual-route perspective on poor reading in a regular orthography: An fMRI study , 2010, Cortex.

[62]  P. H. Seymour,et al.  Foundation literacy acquisition in European orthographies. , 2003, British journal of psychology.

[63]  A. Grabowska,et al.  Implicit phonological and semantic processing in children with developmental dyslexia: Evidence from event-related potentials , 2010, Neuropsychologia.

[64]  T. Münte,et al.  Semantic, syntactic, and phonological processing of written words in adult developmental dyslexic readers: an event-related brain potential study , 2007, BMC Neuroscience.

[65]  P. Skudlarski,et al.  Disruption of posterior brain systems for reading in children with developmental dyslexia , 2002, Biological Psychiatry.

[66]  J. Fletcher,et al.  Cerebral mechanisms involved in word reading in dyslexic children: a magnetic source imaging approach. , 2000, Cerebral cortex.

[67]  M. D’Esposito Working memory. , 2008, Handbook of clinical neurology.

[68]  L. Katz,et al.  Functional neuroimaging studies of reading and reading disability (developmental dyslexia). , 2000, Mental retardation and developmental disabilities research reviews.