Cortical networks for vision and language in dyslexic and normal children of variable socio-economic status

In dyslexia, anomalous activations have been described in both left temporo-parietal language cortices and in left ventral visual occipito-temporal cortex. However, the reproducibility, task-dependency, and presence of these brain anomalies in childhood rather than adulthood remain debated. We probed the large-scale organization of ventral visual and spoken language areas in dyslexic children using minimal target-detection tasks that were performed equally well by all groups. In 23 normal and 23 dyslexic 10-year-old children from two different socio-economic status (SES) backgrounds, we compared fMRI activity to visually presented houses, faces, and written strings, and to spoken sentences in the native or in a foreign language. Our results confirm a disorganization of both ventral visual and spoken language areas in dyslexic children. Visually, dyslexic children showed a normal lateral-to-medial mosaic of preferences, as well as normal responses to houses and checkerboards, but a reduced activation to words in the visual word form area (VWFA) and to faces in the right fusiform face area (FFA). Auditorily, dyslexic children exhibited reduced responses to speech in posterior temporal cortex, left insula and supplementary motor area, as well as reduced responses to maternal language in subparts of the planum temporale, left basal language area and VWFA. By correlating these two findings, we identify spoken-language predictors of VWFA activation to written words, which differ for dyslexic and normal readers. Similarities in fMRI deficits in both SES groups emphasize the existence of a core set of brain activation anomalies in dyslexia, regardless of culture, language and SES, without however resolving whether these anomalies are a cause or a consequence of impaired reading.

[1]  Bernard Mazoyer,et al.  Impact of modality and linguistic complexity during reading and listening tasks , 2007, NeuroImage.

[2]  Charles A. Perfetti,et al.  Focusing Attention on Decoding for Children With Poor Reading Skills: Design and Preliminary Tests of the Word Building Intervention , 2003 .

[3]  Masatoshi Itoh,et al.  Recruitment of fusiform face area associated with listening to degraded speech sounds in auditory–visual speech perception: a PET study , 2005, Neuroscience Letters.

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

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

[6]  Karl J. Friston,et al.  A multimodal language region in the ventral visual pathway , 1998, Nature.

[7]  Andreas Kleinschmidt,et al.  Interaction of Face and Voice Areas during Speaker Recognition , 2005, Journal of Cognitive Neuroscience.

[8]  M Ingvar,et al.  The illiterate brain. Learning to read and write during childhood influences the functional organization of the adult brain. , 1998, Brain : a journal of neurology.

[9]  Andreas Kleinschmidt,et al.  Specialization for written words over objects in the visual cortex , 2011, NeuroImage.

[10]  S. Dehaene,et al.  Beyond Hemispheric Dominance: Brain Regions Underlying the Joint Lateralization of Language and Arithmetic to the Left Hemisphere , 2010, Journal of Cognitive Neuroscience.

[11]  Charles B. Mikell,et al.  Categorical speech representation in human superior temporal gyrus. , 2010, Neurosurgery.

[12]  Elise Temple,et al.  Brain mechanisms in normal and dyslexic readers , 2002, Current Opinion in Neurobiology.

[13]  F. Ramus,et al.  From genes to behavior in developmental dyslexia , 2006, Nature Neuroscience.

[14]  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.

[15]  Nonie K. Lesaux,et al.  The development of reading in children who speak English as a second language. , 2003, Developmental psychology.

[16]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[17]  R. Buxton,et al.  The development of face and location processing: an fMRI study , 2003 .

[18]  Valerie A. Carr,et al.  Spatiotemporal Dynamics of Modality-Specific and Supramodal Word Processing , 2003, Neuron.

[19]  Bruce D. McCandliss,et al.  Socioeconomic gradients predict individual differences in neurocognitive abilities. , 2007, Developmental science.

[20]  Guillaume P. Dehaene,et al.  Functional segregation of cortical language areas by sentence repetition , 2006, Human brain mapping.

[21]  R P Lesser,et al.  Characterization of the basal temporal language area in patients with left temporal lobe epilepsy , 1990, Neurology.

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

[23]  Marc Brysbaert,et al.  Cerebral Lateralization of Frontal Lobe Language Processes and Lateralization of the Posterior Visual Word Processing System , 2008, Journal of Cognitive Neuroscience.

[24]  J B Poline,et al.  Cerebral mechanisms of word masking and unconscious repetition priming , 2001, Nature Neuroscience.

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

[26]  J. Ziegler,et al.  Speech-perception-in-noise deficits in dyslexia. , 2009, Developmental science.

[27]  Jane E Joseph,et al.  Progressive and regressive developmental changes in neural substrates for face processing: testing specific predictions of the Interactive Specialization account. , 2011, Developmental science.

[28]  Rafael Malach,et al.  Large-Scale Mirror-Symmetry Organization of Human Occipito-Temporal Object Areas , 2003, Neuron.

[29]  K. Seki,et al.  The efficacy of kinesthetic reading treatment for pure alexia , 1995, Neuropsychologia.

[30]  Bernard Lété,et al.  MANULEX: A grade-level lexical database from French elementary school readers , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[31]  Leslie G. Ungerleider,et al.  Distributed representation of objects in the human ventral visual pathway. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Bruce D. McCandliss,et al.  Fast, visual specialization for reading in English revealed by the topography of the N170 ERP response , 2005, Behavioral and Brain Functions.

[33]  Patrik Vuilleumier,et al.  Differential development of selectivity for faces and bodies in the fusiform gyrus. , 2009, Developmental science.

[34]  S. Dehaene,et al.  How Learning to Read Changes the Cortical Networks for Vision and Language , 2010, Science.

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

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

[37]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[38]  M. Seghier,et al.  An anatomical signature for literacy , 2009, Nature.

[39]  Bruce D. McCandliss,et al.  The development of reading impairment: a cognitive neuroscience model. , 2003, Mental retardation and developmental disabilities research reviews.

[40]  Michael S Beauchamp,et al.  Neural Correlates of Interindividual Differences in Children's Audiovisual Speech Perception , 2011, The Journal of Neuroscience.

[41]  F Fazio,et al.  Regional reductions of gray matter volume in familial dyslexia , 2004, Neurology.

[42]  Martin Kronbichler,et al.  Meta-analyzing brain dysfunctions in dyslexic children and adults , 2011, NeuroImage.

[43]  Dries J. W. Froyen,et al.  Multi-sensory learning and learning to read. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[44]  Mark A. Eckert,et al.  Anatomical Signatures of Dyslexia in Children: Unique Information from Manual and Voxel Based Morphometry Brain Measures , 2005, Cortex.

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

[46]  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.

[47]  Talma Hendler,et al.  Eccentricity Bias as an Organizing Principle for Human High-Order Object Areas , 2002, Neuron.

[48]  Pierre Lefavrais,et al.  Manuel du test de l'alouette : test d'analyse de la lecture et de la dyslexie , 1967 .

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

[50]  H. Lüders,et al.  Basal temporal language area. , 1991, Brain : a journal of neurology.

[51]  Zane Z. Zheng,et al.  The functional specialization of the planum temporale. , 2009, Journal of neurophysiology.

[52]  Joel Fluss,et al.  Poor Reading in French Elementary School: The Interplay of Cognitive, Behavioral, and Socioeconomic Factors , 2009, Journal of developmental and behavioral pediatrics : JDBP.

[53]  Jean-François Démonet,et al.  The graphemic/motor frontal area Exner's area revisited , 2009, Annals of neurology.

[54]  Andrew N. Meltzoff,et al.  Brain Activation during Face Perception: Evidence of a Developmental Change , 2005, Journal of Cognitive Neuroscience.

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

[56]  J. Fletcher,et al.  Specific reading disability (dyslexia): what have we learned in the past four decades? , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[57]  Bruce D. McCandliss,et al.  Socioeconomic background modulates cognition-achievement relationships in reading. , 2006, Cognitive development.

[58]  Jean-Luc Velay,et al.  Visual presentation of single letters activates a premotor area involved in writing , 2003, NeuroImage.

[59]  N. Kraus,et al.  Context-Dependent Encoding in the Human Auditory Brainstem Relates to Hearing Speech in Noise: Implications for Developmental Dyslexia , 2009, Neuron.

[60]  Bruce D. McCandliss,et al.  Development of Visual Expertise for Reading: Rapid Emergence of Visual Familiarity for an Artificial Script , 2010, Developmental neuropsychology.

[61]  Jean-Claude Gilhodes,et al.  Learning through Hand- or Typewriting Influences Visual Recognition of New Graphic Shapes: Behavioral and Functional Imaging Evidence , 2008, Journal of Cognitive Neuroscience.

[62]  D. Burnham,et al.  Impact of language on development of auditory-visual speech perception. , 2008, Developmental science.

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

[64]  Johannes C. Ziegler,et al.  Orthographic effects in spoken language: On-line activation or phonological restructuring? , 2009, Brain Research.

[65]  J. Rumsey,et al.  Failure to activate the left temporoparietal cortex in dyslexia. An oxygen 15 positron emission tomographic study. , 1992, Archives of neurology.

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

[67]  Pascale Colé,et al.  French normative data on reading and related skills from EVALEC, a new computerized battery of tests (end Grade 1, Grade 2, Grade 3, and Grade 4) , 2005 .

[68]  Daniel A. Hackman,et al.  Socioeconomic Status and the Developing Brain , 2022 .

[69]  Martin Kronbichler,et al.  Developmental dyslexia: Gray matter abnormalities in the occipitotemporal cortex , 2008, Human brain mapping.

[70]  Uta Frith,et al.  Identifying dyslexia in bilingual children: a phonological approach with inner London Sylheti speakers , 1998 .

[71]  Peter T Fox,et al.  Cognitive processing in Chinese literate and illiterate subjects: An fMRI study , 2006, Human brain mapping.

[72]  Beatriz Luna,et al.  Cerebral Cortex doi:10.1093/cercor/bhq269 ‘‘What’ ’ Precedes ‘‘Which’’: Developmental Neural Tuning in Face- and Place-Related Cortex , 2011 .

[73]  R. Goebel,et al.  Reduced Neural Integration of Letters and Speech Sounds Links Phonological and Reading Deficits in Adult Dyslexia , 2009, Current Biology.

[74]  James R. Booth,et al.  Children with reading difficulties show differences in brain regions associated with orthographic processing during spoken language processing , 2010, Brain Research.

[75]  R. Goebel,et al.  Integration of Letters and Speech Sounds in the Human Brain , 2004, Neuron.

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

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

[78]  Roland Sparing,et al.  The dorsal premotor cortex orchestrates concurrent speech and fingertapping movements , 2009, The European journal of neuroscience.

[79]  E. Gentaz,et al.  The visuo-haptic and haptic exploration of letters increases the kindergarten-children's understanding of the alphabetic principle , 2004 .

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

[81]  D. LeBihan,et al.  Phonological Grammar Shapes the Auditory Cortex: A Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

[82]  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.

[83]  P. McGuire,et al.  Cortical substrates for the perception of face actions: an fMRI study of the specificity of activation for seen speech and for meaningless lower-face acts (gurning). , 2001, Brain research. Cognitive brain research.

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

[85]  K. Grill-Spector,et al.  Differential development of high-level visual cortex correlates with category-specific recognition memory , 2007, Nature Neuroscience.

[86]  B. Argall,et al.  Unraveling multisensory integration: patchy organization within human STS multisensory cortex , 2004, Nature Neuroscience.

[87]  Joseph K. Torgesen,et al.  Longitudinal Studies of Phonological Processing and Reading , 1994, Journal of learning disabilities.

[88]  K. Eklund,et al.  Early development of children at familial risk for dyslexia--follow-up from birth to school age. , 2004, Dyslexia.

[89]  P. Bertelson,et al.  Does awareness of speech as a sequence of phones arise spontaneously? , 1979, Cognition.

[90]  Bruce D. McCandliss,et al.  Brain-behavior relationships in reading acquisition are modulated by socioeconomic factors. , 2006, Developmental science.

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

[92]  Urs Maurer,et al.  Auditory Selective Attention to Speech Modulates Activity in the Visual Word Form Area , 2009, Cerebral cortex.

[93]  Stanislas Dehaene,et al.  Task-specific change of unconscious neural priming in the cerebral language network , 2007, Proceedings of the National Academy of Sciences.

[94]  T. Mexia,et al.  Author ' s personal copy , 2009 .

[95]  Steven L. Small,et al.  Neural development of networks for audiovisual speech comprehension , 2010, Brain and Language.

[96]  Leslie G. Ungerleider,et al.  The Representation of Objects in the Human Occipital and Temporal Cortex , 2000, Journal of Cognitive Neuroscience.

[97]  F. Ramus Neurobiology of dyslexia: a reinterpretation of the data. , 2004, Trends in neurosciences.

[98]  Isabelle Jambaqué,et al.  Épreuves de fluence verbale et de dénomination chez l'enfant d'âge scolaire , 2000 .

[99]  Marc Brysbaert,et al.  The left ventral occipito-temporal response to words depends on language lateralization but not on visual familiarity. , 2010, Cerebral cortex.

[100]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[101]  Dries J. W. Froyen,et al.  Evidence for a specific cross-modal association deficit in dyslexia: an electrophysiological study of letter-speech sound processing. , 2011, Developmental science.

[102]  R Salmelin,et al.  Category-specific occipitotemporal activation during face perception in dyslexic individuals: an MEG study , 2003, NeuroImage.

[103]  Beatriz Luna,et al.  Visual category-selectivity for faces, places and objects emerges along different developmental trajectories. , 2007, Developmental science.

[104]  J. Velay,et al.  The influence of writing practice on letter recognition in preschool children: a comparison between handwriting and typing. , 2005, Acta psychologica.

[105]  N. Geschwind,et al.  Developmental dyslexia: Four consecutive patients with cortical anomalies , 1985, Annals of neurology.

[106]  B. Mazoyer,et al.  A Common Language Network for Comprehension and Production: A Contribution to the Definition of Language Epicenters with PET , 2000, NeuroImage.

[107]  David B. Pisoni,et al.  Neural processing of asynchronous audiovisual speech perception , 2010, NeuroImage.

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

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

[110]  Franck Ramus,et al.  Dyslexie, dysorthographie, dyscalculie : bilan des données scientifiques , 2007 .

[111]  Urs Maurer,et al.  Attentional Focus During Learning Impacts N170 ERP Responses to an Artificial Script , 2010, Developmental neuropsychology.

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

[113]  H. Lüders,et al.  Evidence for a basal temporal visual language center , 2008, Neurology.