Print-specific multimodal brain activation in kindergarten improves prediction of reading skills in second grade

Children who are poor readers usually experience troublesome school careers and consequently often suffer from secondary emotional and behavioural problems. Early identification and prediction of later reading problems thus are critical in order to start targeted interventions for those children with an elevated risk for emerging reading problems. In this study, behavioural precursors of reading were assessed in nineteen (aged 6.4 ± 0.3 years) non-reading kindergarteners before training letter-speech sound associations with a computerized game (Graphogame) for eight weeks. The training aimed to introduce the basic principles of letter-speech sound correspondences and to initialize the sensitization of specific brain areas to print. Event-related potentials (ERP) and functional magnetic resonance imaging (fMRI) data were recorded during an explicit word/symbol processing task after the training. Reading skills were assessed two years later in second grade. The focus of this study was on clarifying whether electrophysiological and fMRI data of kindergarten children significantly improve prediction of future reading skills in 2nd grade over behavioural data alone. Based on evidence from previous studies demonstrating the importance of initial print sensitivity in the left occipito-temporal visual word form system (VWFS) for learning to read, the first pronounced difference in processing words compared to symbols in the ERP, an occipito-temporal negativity (N1: 188-281 ms) along with the corresponding functional activation in the left occipito-temporal VWFS were defined as potential predictors. ERP and fMRI data in kindergarteners significantly improved the prediction of reading skills in 2nd grade over behavioural data alone. Together with the behavioural measures they explained up to 88% of the variance. An additional discriminant analysis revealed a remarkably high accuracy in classifying normal (n=11) and poor readers (n=6). Due to the key limitation of the study, i.e. the small group sizes, the results of our prediction analyses should be interpreted with caution and regarded as preliminary despite cross-validation. Nevertheless our results indicate the potential of combining neuroimaging and behavioural measures to improve prediction at an early stage, when literacy skills are acquired and interventions are most beneficial.

[1]  John C Gore,et al.  Neural systems for compensation and persistence: young adult outcome of childhood reading disability , 2003, Biological Psychiatry.

[2]  Qian Luo,et al.  Neural basis of the non‐attentional processing of briefly presented words , 2003, Human brain mapping.

[3]  Heikki Lyytinen,et al.  Event-Related Potentials and Consonant Differentiation in Newborns with Familial Risk for Dyslexia , 2001, Journal of learning disabilities.

[4]  B. Pennington,et al.  Early reading development in children at family risk for dyslexia. , 2001, Child development.

[5]  P. Wolff,et al.  Rate variables and automatized naming in developmental dyslexia , 1990, Brain and Language.

[6]  W. Schneider Introduction: The early prediction of reading and spelling , 1993 .

[7]  H. Lyytinen,et al.  Brain sensitivity to print emerges when children learn letter–speech sound correspondences , 2010, Proceedings of the National Academy of Sciences.

[8]  K. Eklund,et al.  Brain Event-Related Potentials (ERPs) Measured at Birth Predict Later Language Development in Children with and Without Familial Risk for Dyslexia , 2005, Cortex.

[9]  I. Kanazawa,et al.  Different cortical activity in reading of Kanji words, Kana words and Kana nonwords. , 2000, Brain research. Cognitive brain research.

[10]  H. Wimmer,et al.  The relationship of phonemic awareness to reading acquisition: More consequence than precondition but still important , 1991, Cognition.

[11]  Stefan Samuelsson,et al.  Preschool cognitive and language skills predicting Kindergarten and Grade 1 reading and spelling: a cross-linguistic comparison , 2009 .

[12]  Stefan Samuelsson,et al.  Predicting reading and spelling difficulties in transparent and opaque orthographies: a comparison between Scandinavian and US/Australian children. , 2010, Dyslexia.

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

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

[15]  G Jobard,et al.  Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies , 2003, NeuroImage.

[16]  H. Lyytinen,et al.  In search of a science-based application: a learning tool for reading acquisition. , 2009, Scandinavian journal of psychology.

[17]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[18]  B. Pennington,et al.  Reliability and Validity of the Adult Reading History Questionnaire , 2000, Journal of learning disabilities.

[19]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[20]  J. Tomblin,et al.  Estimating the Risk of Future Reading Difficulties in Kindergarten Children: A Research-Based Model and Its Clinical Implementation. , 2001, Language, speech, and hearing services in schools.

[21]  A Cornwall,et al.  The Relationship Between Phonological Awareness and Reading and Spelling Achievement Eleven Years Later , 1995, Journal of learning disabilities.

[22]  R. Olson,et al.  Are RAN- and phonological awareness-deficits additive in children with reading disabilities? , 2001, Dyslexia.

[23]  Heikki Lyytinen,et al.  Very early phonological and language skills: estimating individual risk of reading disability. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[24]  H. Lyytinen,et al.  Event-related potentials in newborns with and without familial risk for dyslexia: principal component analysis reveals differences between the groups , 2003, Journal of Neural Transmission.

[25]  R. Savage,et al.  Evidence of a highly specific relationship between rapid automatic naming of digits and text-reading speed , 2005, Brain and Language.

[26]  W. Schneider,et al.  THE EARLY PREDICTION OF READING AND SPELLING: EVIDENCE FROM THE MUNICH LONGITUDINAL STUDY ON THE GENESIS OF INDIVIDUAL COMPETENCIES , 1997 .

[27]  G. Hynd,et al.  Prediction of group membership in developmental dyslexia, attention deficit hyperactivity disorder, and normal controls using brain morphometric analysis of magnetic resonance imaging. , 1996, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

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

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

[30]  J. Hart,et al.  Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. , 2003, Brain research. Cognitive brain research.

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

[32]  F. Manis,et al.  Naming Speed, Phonological Awareness, and Orthographic Knowledge in Second Graders , 2000, Journal of learning disabilities.

[33]  Linnea C. Ehri,et al.  Grapheme-phoneme knowledge is essential for learning to read words in English , 1998 .

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

[35]  R. Wagner,et al.  The nature of phonological processing and its causal role in the acquisition of reading skills. , 1987 .

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

[37]  D. Brandeis,et al.  Neurophysiology in Preschool Improves Behavioral Prediction of Reading Ability Throughout Primary School , 2009, Biological Psychiatry.

[38]  Tali Bitan,et al.  Neural correlates of mapping from phonology to orthography in children performing an auditory spelling task. , 2007, Developmental science.

[39]  H. Lyytinen,et al.  Computer-assisted remedial reading intervention for school beginners at risk for reading disability. , 2011, Child development.

[40]  H. Pashler,et al.  Puzzlingly High Correlations in fMRI Studies of Emotion, Personality, and Social Cognition 1 , 2009, Perspectives on psychological science : a journal of the Association for Psychological Science.

[41]  D. Compton Modeling the response of normally achieving and at-risk first grade children to word reading instruction , 2000, Annals of dyslexia.

[42]  Z. Gou,et al.  The infant as a prelinguistic model for language learning impairments: Predicting from event-related potentials to behavior , 2006, Neuropsychologia.

[43]  Kaisa Aunola,et al.  Development of Reading and Spelling Finnish From Preschool to Grade 1 and Grade 2 , 2006 .

[44]  G. Albertini,et al.  Internalizing correlates of dyslexia , 2009, World journal of pediatrics : WJP.

[45]  S. Dehaene,et al.  Computer-Assisted Intervention for Children with Low Numeracy Skills , 2009 .

[46]  Philippe Pinel,et al.  Cortical representations of symbols, objects, and faces are pruned back during early childhood. , 2011, Cerebral cortex.

[47]  M Coltheart,et al.  DRC: a dual route cascaded model of visual word recognition and reading aloud. , 2001, Psychological review.

[48]  Emily B. Myers,et al.  Recruitment of anterior and posterior structures in lexical–semantic processing: An fMRI study comparing implicit and explicit tasks , 2008, Brain and Language.

[49]  B. Horwitz,et al.  Phonological and orthographic components of word recognition. A PET-rCBF study. , 1997, Brain : a journal of neurology.

[50]  B. Reboussin,et al.  Severity of Emotional and Behavioral Problems Among Poor and Typical Readers , 2005, Journal of abnormal child psychology.

[51]  Maria Chang,et al.  Structural brain alterations associated with dyslexia predate reading onset , 2011, NeuroImage.

[52]  D. Irblich Klicpera, C.; Schabmann, A.; Gasteiger-Klicpera, B. (2003): Legasthenie. Modelle, Diagnose, Therapie und Förderung. München: Reinhardt (316 Seiten; € 23,90) [Rezension] , 2004 .

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

[54]  P. Bryant,et al.  Categorizing sounds and learning to read—a causal connection , 1983, Nature.

[55]  Ulla Richardson,et al.  Early emergence of deviant frontal fMRI activity for phonological processes in poor beginning readers , 2010, NeuroImage.

[56]  D. Schacter,et al.  A sensory signature that distinguishes true from false memories , 2004, Nature Neuroscience.

[57]  D. Shankweiler,et al.  Explicit Syllable and Phoneme Segmentation in the Young Child , 1974 .

[58]  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.

[59]  Helmut Remschmidt,et al.  Auditory processing and dyslexia: evidence for a specific speech processing deficit , 1998, Neuroreport.

[60]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

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

[62]  D. Poeppel,et al.  Towards a functional neuroanatomy of speech perception , 2000, Trends in Cognitive Sciences.

[63]  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.

[64]  A. H. Mack Developmental dyslexia in Chinese and English populations: dissociating the effect of dyslexia from language differences , 2011 .

[65]  James R. Booth,et al.  Weaker top–down modulation from the left inferior frontal gyrus in children , 2006, NeuroImage.

[66]  Stephen R. Burgess,et al.  Relations of the home literacy environment (HLE) to the development of reading-related abilities: A one-year longitudinal study , 2002 .

[67]  George K. Georgiou,et al.  Predictors of word decoding and reading fluency across languages varying in orthographic consistency. , 2008 .

[68]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

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

[70]  Turid Helland,et al.  Brain activation on pre-reading tasks reveals at-risk status for dyslexia in 6-year-old children. , 2009, Scandinavian journal of psychology.

[71]  R. Frackowiak,et al.  Demonstrating the implicit processing of visually presented words and pseudowords. , 1996, Cerebral cortex.

[72]  Bruce D. McCandliss,et al.  Neural systems predicting long-term outcome in dyslexia , 2010, Proceedings of the National Academy of Sciences.

[73]  John D E Gabrieli,et al.  Prediction of children's reading skills using behavioral, functional, and structural neuroimaging measures. , 2007, Behavioral neuroscience.

[74]  Stephen R. Burgess,et al.  Changing relations between phonological processing abilities and word-level reading as children develop from beginning to skilled readers: a 5-year longitudinal study. , 1997, Developmental psychology.

[75]  G. Whitehurst,et al.  Child development and emergent literacy. , 1998, Child development.

[76]  H. Lyytinen,et al.  Early identification of dyslexia and the use of computer game-based practice to support reading acquisition , 2007 .

[77]  Heikki Lyytinen,et al.  The development of children at familial risk for dyslexia: Birth to early school age , 2004, Annals of dyslexia.

[78]  D. Molfese Predicting Dyslexia at 8 Years of Age Using Neonatal Brain Responses , 2000, Brain and Language.

[79]  Daniel Brandeis,et al.  Altered responses to tone and phoneme mismatch in kindergartners at familial dyslexia risk , 2003, Neuroreport.

[80]  Mariano Sigman,et al.  Hierarchical Coding of Letter Strings in the Ventral Stream: Dissecting the Inner Organization of the Visual Word-Form System , 2007, Neuron.

[81]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[82]  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.

[83]  T. Sejnowski,et al.  Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects , 2000, Clinical Neurophysiology.

[84]  Mark S. Seidenberg,et al.  On the bases of two subtypes of development dyslexia , 1996, Cognition.

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

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

[87]  K. Eklund,et al.  Newborn Event-Related Potentials Predict Poorer Pre-Reading Skills in Children at Risk for Dyslexia , 2010, Journal of learning disabilities.