Reading for sound with dyslexia: Evidence for early orthographic and late phonological integration deficits

Deteriorated phonological representations are widely assumed to be the underlying cause of reading difficulties in developmental dyslexia; however, existing evidence also implicates degraded orthographic processing. Here, we used event-related potentials whilst dyslexic and control adults performed a pseudoword-word priming task requiring deep phonological analysis to examine phonological and orthographic priming, respectively. Pseudowords were manipulated to be homophonic or non-homophonic to a target word and more or less orthographically similar. Since previous ERP research with normal readers has established phonologically driven differences as early as 250 ms from word presentation, degraded phonological representations were expected to reveal reduced phonological priming in dyslexic readers from 250 ms after target word onset. However, phonological priming main effects in both the N2 and P3 ranges were indistinguishable in amplitude between groups. Critically, we found group differences in the N1 range, such that orthographic modulations observed in controls were absent in the dyslexic group. Furthermore, early group differences in phonological priming transpired as interactions with orthographic priming (in P2, N2 and P3 ranges). A group difference in phonological priming did not emerge until the P600 range, in which the dyslexic group showed significantly attenuated priming. As the P600 is classically associated with online monitoring and reanalysis, this pattern of results suggest that during deliberate phonological processing, the phonological deficit in reading may relate more to inefficient monitoring rather than deficient detection. Meanwhile, early differences in perceptual processing of phonological information may be driven by the strength of engagement with orthographic information.

[1]  R. Goebel,et al.  Deviant processing of letters and speech sounds as proximate cause of reading failure: a functional magnetic resonance imaging study of dyslexic children. , 2010, Brain : a journal of neurology.

[2]  J. Ashby,et al.  Prosodic phonological representations early in visual word recognition. , 2008, Journal of experimental psychology. Human perception and performance.

[3]  F. Ramus,et al.  Developmental dyslexia : specific phonological deficit or general sensorimotor dysfunction ? , 2003 .

[4]  M. Bruck Persistence of dyslexics' phonological awareness deficits. , 1992 .

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

[6]  U. Goswami,et al.  Phonological representations, reading development and dyslexia: towards a cross-linguistic theoretical framework. , 2000, Dyslexia.

[7]  Richard S. J. Frackowiak,et al.  Is developmental dyslexia a disconnection syndrome? Evidence from PET scanning. , 1996, Brain : a journal of neurology.

[8]  H. Kolk,et al.  Structure and limited capacity in verbal working memory: A study with event-related potentials , 2003, Brain and Language.

[9]  T. Givón,et al.  Brain Plasticity in Learning Visual Words , 1997, Cognitive Psychology.

[10]  H. Wimmer,et al.  Children with dyslexia and right parietal lobe dysfunction: event-related potentials in response to words and pseudowords , 2002, Neuroscience Letters.

[11]  Silvia Brem,et al.  The left occipitotemporal system in reading: Disruption of focal fMRI connectivity to left inferior frontal and inferior parietal language areas in children with dyslexia , 2011, NeuroImage.

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

[13]  G. Thierry,et al.  P300 investigation of phoneme change detection in dyslexic adults , 2004, Neuroscience Letters.

[14]  Merav Ahissar,et al.  Auditory processing deficits in dyslexia: task or stimulus related? , 2005, Cerebral cortex.

[15]  J. Connolly,et al.  Influence of phonological expectations during a phoneme deletion task: evidence from event-related brain potentials. , 2003, Psychophysiology.

[16]  J. Booth,et al.  Children with Reading Disability Show Brain Differences in Effective Connectivity for Visual, but Not Auditory Word Comprehension , 2010, PloS one.

[17]  G. Thierry,et al.  Literate humans sound out words during silent reading , 2011, Neuroreport.

[18]  P. Holcomb Semantic priming and stimulus degradation: implications for the role of the N400 in language processing. , 2007, Psychophysiology.

[19]  Kristi A. Kiyonaga,et al.  The time course of orthographic and phonological code activation. , 1993, Psychological science.

[20]  Angela D. Friederici,et al.  Working Memory and Lexical Ambiguity Resolution as Revealed by ERPs: A Difficult Case for Activation Theories , 2003, Journal of Cognitive Neuroscience.

[21]  Max Coltheart,et al.  The MRC Psycholinguistic Database , 1981 .

[22]  Nonie K. Lesaux,et al.  Persistence of Phonological Processing Deficits in College Students with Dyslexia Who Have Age-Appropriate Reading Skills , 2001, Journal of learning disabilities.

[23]  Jose Morais,et al.  Levels of phonological representation in skilled reading and in learning to read , 2003 .

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

[25]  J. Connolly,et al.  Event-Related Potential Components Reflect Phonological and Semantic Processing of the Terminal Word of Spoken Sentences , 1994, Journal of Cognitive Neuroscience.

[26]  Trichur Raman Vidyasagar,et al.  Dyslexia: a deficit in visuo-spatial attention, not in phonological processing , 2010, Trends in Cognitive Sciences.

[27]  Andrea Mechelli,et al.  More than words: a common neural basis for reading and naming deficits in developmental dyslexia? , 2004, Brain : a journal of neurology.

[28]  S. Valdois,et al.  Influence of the visual attention span on child reading performance: A cross-sectional study , 2009 .

[29]  Peter Hagoort,et al.  The Processing Nature of the N400: Evidence from Masked Priming , 1993, Journal of Cognitive Neuroscience.

[30]  B. Pennington,et al.  Deficient implicit phonological representations in children with dyslexia. , 2006, Journal of experimental child psychology.

[31]  Bruce A. Crum Comparison of the Reading Subtests of The Woodcock Johnson Tests of Achievement- Third Edition and the Wechsler Individual Achievement Test-Second Edition , 2006 .

[32]  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.

[33]  Régine Kolinsky,et al.  Perception and awareness in phonological processing: the case of the phoneme , 1994, Cognition.

[34]  H. Renvall,et al.  Impaired processing of rapid stimulus sequences in dyslexia , 2001, Trends in Cognitive Sciences.

[35]  Jonathan Grainger,et al.  On the Time Course of Visual Word Recognition: An Event-related Potential Investigation using Masked Repetition Priming , 2006, Journal of Cognitive Neuroscience.

[36]  M. Zorzi,et al.  The relationship between visuo-spatial attention and nonword reading in developmental dyslexia , 2006, Cognitive neuropsychology.

[37]  Curt von Euler,et al.  Residual differences in language processing in compensated dyslexics revealed in simple word reading tasks , 2002, Brain and Language.

[38]  Jamie L. Metsala,et al.  Spoken Word Recognition in Reading Disabled Children. , 1997 .

[39]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

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

[41]  G. Schulte-Körne,et al.  Clinical neurophysiology of visual and auditory processing in dyslexia: A review , 2010, Clinical Neurophysiology.

[42]  H. Wimmer,et al.  Impaired visual processing of letter and digit strings in adult dyslexic readers , 2006, Vision Research.

[43]  G. Thierry,et al.  Phonological oddballs in the focus of attention elicit a normal P3b in dyslexic adults. , 2005, Brain research. Cognitive brain research.

[44]  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.

[45]  Zvia Breznitz,et al.  Can the Error Detection Mechanism Benefit from Training the Working Memory? A Comparison between Dyslexics and Controls — An ERP Study , 2009, PloS one.

[46]  F. Zwarts,et al.  Brain responses to subject-verb agreement violations in spoken language in developmental dyslexia: an ERP study. , 2006, Dyslexia.

[47]  Tzipi Horowitz-Kraus,et al.  An error-detection mechanism in reading among dyslexic and regular readers – An ERP study , 2008, Clinical Neurophysiology.

[48]  S. Valdois,et al.  Developmental dyslexia: The visual attention span deficit hypothesis , 2007, Cognition.

[49]  Trichur Raman Vidyasagar Neural underpinnings of dyslexia as a disorder of visuo‐spatial attention , 2004, Clinical & experimental optometry.

[50]  U. Frith,et al.  Explicit and implicit processing of words and pseudowords by adult developmental dyslexics: A search for Wernicke's Wortschatz? , 1999, Brain : a journal of neurology.

[51]  H. Kolk,et al.  Late positivities in unusual situations , 2007, Brain and Language.

[52]  J. Démonet,et al.  Superior parietal lobule dysfunction in a homogeneous group of dyslexic children with a visual attention span disorder , 2011, Brain and Language.

[53]  Donna Coch,et al.  Word and pseudoword superiority effects reflected in the ERP waveform , 2010, Brain Research.

[54]  B L Lambert,et al.  Similarity as a risk factor in drug-name confusion errors: the look-alike (orthographic) and sound-alike (phonetic) model. , 1999, Medical care.

[55]  Don M. Tucker,et al.  A Cognitive-Anatomical Approach to Attention in Lexical Access , 1991, Journal of Cognitive Neuroscience.

[56]  B. Pennington From single to multiple deficit models of developmental disorders , 2006, Cognition.

[57]  John F Connolly,et al.  Separating phonological and semantic processing in auditory sentence processing: A high‐resolution event‐related brain potential study , 2004, Human brain mapping.

[58]  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.

[59]  A. Facoetti,et al.  Different underlying neurocognitive deficits in developmental dyslexia: A comparative study , 2010, Neuropsychologia.

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

[61]  Carsten Elbro,et al.  Early linguistic abilities and reading development: A review and a hypothesis , 1996 .

[62]  S. Valdois,et al.  Preorthographical constraints on visual word recognition: Evidence from a case study of developmental surface dyslexia , 2007, Cognitive neuropsychology.

[63]  F. Ramus,et al.  Exploring dyslexics' phonological deficit I: lexical vs sub-lexical and input vs output processes. , 2005, Dyslexia.

[64]  E Donchin,et al.  Brain potentials as indices of orthographic and phonological interaction during word matching. , 1987, Journal of experimental psychology. Learning, memory, and cognition.

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

[66]  S. Valdois,et al.  The cognitive deficits responsible for developmental dyslexia: review of evidence for a selective visual attentional disorder. , 2004, Dyslexia.

[67]  James R. Booth,et al.  Effective brain connectivity in children with reading difficulties during phonological processing , 2008, Brain and Language.

[68]  S. Crewther,et al.  Towards an understanding of the role of the ‘magnocellular advantage’ in fluent reading , 2008, Neuroscience & Biobehavioral Reviews.

[69]  J. Ziegler,et al.  Pseudohomophone effects provide evidence of early lexico‐phonological processing in visual word recognition , 2009, Human brain mapping.

[70]  M. L. Kelly,et al.  Dyslexic and nondyslexic reading fluency: Rapid automatized naming and the importance of continuous lists , 2009, Psychonomic bulletin & review.

[71]  Judith Rispens,et al.  Syntactic and phonological processing in developmental dyslexia , 2004 .

[72]  B. A. Blachman Foundations of Reading Acquisition and Dyslexia : Implications for Early Intervention , 2013 .

[73]  Colin M. Brown,et al.  The N400 as a function of the level of processing. , 1995, Psychophysiology.

[74]  G. Potts An ERP index of task relevance evaluation of visual stimuli , 2004, Brain and Cognition.

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

[76]  Trichur Raman Vidyasagar,et al.  Integration of the visual and auditory networks in dyslexia: a theoretical perspective , 2005 .

[77]  J. Connolly,et al.  Electrophysiological markers of pre-lexical speech processing: Evidence for bottom–up and top–down effects on spoken word processing , 2009, Biological Psychology.

[78]  J. J. Ryan,et al.  Wechsler Adult Intelligence Scale-III , 2001 .

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

[80]  L. Chelazzi,et al.  Sluggish engagement and disengagement of non-spatial attention in dyslexic children , 2008, Cortex.

[81]  Uta Frith,et al.  Phonological difficulties in high-functioning dyslexics , 1996 .

[82]  H. Kolk,et al.  Monitoring in language perception: The effect of misspellings of words in highly constrained sentences , 2006, Brain Research.

[83]  H. Wimmer,et al.  A Common Left Occipito-Temporal Dysfunction in Developmental Dyslexia and Acquired Letter-By-Letter Reading? , 2010, PloS one.

[84]  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.

[85]  T. Münte,et al.  Recognition Memory for High- and Low-Frequency Words in Adult Normal and Dyslexic Readers: An Event-Related Brain Potential Study , 2003, Journal of clinical and experimental neuropsychology.

[86]  V. Hazan,et al.  Speech Perception in Children with Specific Reading Difficulties (Dyslexia) , 1998, The Quarterly journal of experimental psychology. A, Human experimental psychology.

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

[88]  M. Coltheart,et al.  The relationship between language-processing and visual-processing deficits in developmental dyslexia , 1999, Cognition.

[89]  D. Bishop,et al.  Using mismatch negativity to study central auditory processing in developmental language and literacy impairments: where are we, and where should we be going? , 2007, Psychological bulletin.

[90]  Michele T. Diaz,et al.  Electrophysiological differentiation of phonological and semantic integration in word and sentence contexts , 2007, Brain Research.

[91]  Chia-Ying Lee,et al.  Orthographic combinability and phonological consistency effects in reading Chinese phonograms: An event-related potential study , 2009, Brain and Language.

[92]  Shelley Miller-Shaul,et al.  The characteristics of young and adult dyslexics readers on reading and reading related cognitive tasks as compared to normal readers. , 2005, Dyslexia.

[93]  Michael A. Ford,et al.  Can I have a quick word? Early electrophysiological manifestations of psycholinguistic processes revealed by event-related regression analysis of the EEG , 2009, Biological Psychology.

[94]  Dorothee J. Chwilla,et al.  Monitoring in language perception: Evidence from ERPs in a picture–sentence matching task , 2008, Neuropsychologia.

[95]  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.

[96]  Heinz Wimmer,et al.  When does the brain register deviances from standard word spellings?--An ERP study. , 2004, Brain research. Cognitive brain research.

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

[98]  H. Wimmer,et al.  Impaired visual processing of multi-element arrays is associated with increased number of eye movements in dyslexic reading , 2005, Vision Research.

[99]  J. Connolly,et al.  The effects of phonological and semantic features of sentence-ending words on visual event-related brain potentials. , 1995, Electroencephalography and clinical neurophysiology.

[100]  T. Münte,et al.  Cognitive brain potentials to novel acoustic stimuli in adult dyslexic readers. , 2002, Dyslexia.

[101]  Dorothee J. Chwilla,et al.  Monitoring in Language Perception: Mild and Strong Conflicts Elicit Different ERP Patterns , 2010, Journal of Cognitive Neuroscience.

[102]  U. Goswami,et al.  Phonological awareness deficits in developmental dyslexia and the phonological representations hypothesis. , 1997, Journal of experimental child psychology.

[103]  H. Remschmidt,et al.  Neurophysiological correlates of word recognition in dyslexia , 2004, Journal of Neural Transmission.

[104]  B. Shaywitz,et al.  A definition of dyslexia , 2003 .

[105]  S. Sereno,et al.  Context Effects in Word Recognition , 2003, Psychological science.

[106]  K. Uutela,et al.  Impaired visual word processing in dyslexia revealed with magnetoencephalography , 1996, Annals of neurology.

[107]  John F Connolly,et al.  Determining the role of phonology in silent reading using event-related brain potentials. , 2004, Brain research. Cognitive brain research.

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

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

[110]  Bernadette M. Jansma,et al.  Neural aspects of cohort-size reduction during visual gating , 2007, Brain Research.

[111]  Andrea Facoetti,et al.  Multisensory Spatial Attention Deficits Are Predictive of Phonological Decoding Skills in Developmental Dyslexia , 2010, Journal of Cognitive Neuroscience.

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

[113]  Gary J. Robertson,et al.  Wide‐Range Achievement Test , 2010 .

[114]  Joseph Dien,et al.  The neurocognitive basis of reading single words as seen through early latency ERPs: A model of converging pathways , 2009, Biological Psychology.

[115]  S. Brady,et al.  Ability to encode phonological representations: An underlying difficulty of poor readers. , 1997 .

[116]  D. R. Smith,et al.  CHAPTER 6 – Wechsler Individual Achievement Test , 2001 .

[117]  Alice Mado Proverbio,et al.  From Orthography to Phonetics: ERP Measures of Grapheme-to-Phoneme Conversion Mechanisms in Reading , 2004, Journal of Cognitive Neuroscience.

[118]  S. Valdois,et al.  Sequential or simultaneous visual processing deficit in developmental dyslexia? , 2008, Vision Research.

[119]  Jonathan Grainger,et al.  Watching the Word Go by: On the Time-course of Component Processes in Visual Word Recognition , 2009, Lang. Linguistics Compass.

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

[121]  Charles Hulme,et al.  Deficits in output phonology: an explanation of reading failure? Cognit , 1992 .

[122]  M. L. Kelly,et al.  Visual deficits in developmental dyslexia: relationships between non-linguistic visual tasks and their contribution to components of reading. , 2008, Dyslexia.