Emergence of the neural network for reading in five-year-old beginning readers of different levels of pre-literacy abilities: An fMRI study

The present study traced the emergence of the neural circuits for reading in five-year-old children of diverse pre-literacy ability. In the fall and winter of kindergarten, children performed a one-back task with letter versus false font stimuli during fMRI scanning. At the start of kindergarten, children with on-track pre-literacy skills (OT) recruited bilateral temporo-parietal regions for the letter > false font comparison. In contrast, children at-risk for reading difficulty (AR) showed no differential activation in this region. Following 3 months of kindergarten and, for AR children, supplemental reading instruction, OT children showed left-lateralized activation in the temporo-parietal region, whereas AR children showed bilateral activation and recruitment of frontal regions including the anterior cingulate cortex. These data suggest that typical reading development is associated with initial recruitment and subsequent disengagement of right hemisphere homologous regions while atypical reading development may be associated with compensatory recruitment of frontal regions.

[1]  R. N. Davis,et al.  Dyslexia-specific brain activation profile becomes normal following successful remedial training , 2002, Neurology.

[2]  S C Cramer,et al.  Instructional treatment associated with changes in brain activation in children with dyslexia , 2003, Neurology.

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

[4]  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.

[5]  T. Braver,et al.  Cognitive Neuroscience Approaches to Individual Differences in Working Memory and Executive Control: Conceptual and Methodological Issues , 2010 .

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

[7]  Helen J. Neville,et al.  Proficiency Differences in Syntactic Processing of Monolingual Native Speakers Indexed by Event-related Potentials , 2010, Journal of Cognitive Neuroscience.

[8]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[9]  Helen J. Neville,et al.  Language comprehension and cerebral specialization from 13 to 20 months , 1997 .

[10]  Steven L. Miller,et al.  Neural deficits in children with dyslexia ameliorated by behavioral remediation: Evidence from functional MRI , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

[12]  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.

[13]  Greg J. Duncan,et al.  "School readiness and later achievement": Correction to Duncan et al. (2007). , 2008 .

[14]  C. Blair,et al.  School readiness. Integrating cognition and emotion in a neurobiological conceptualization of children's functioning at school entry. , 2002, The American psychologist.

[15]  S E Shaywitz,et al.  Neurobiological studies of reading and reading disability. , 2001, Journal of communication disorders.

[16]  Jean-Noël Foulin.  Why is letter-name knowledge such a good predictor of learning to read? , 2005 .

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

[18]  A. Kelly,et al.  Human functional neuroimaging of brain changes associated with practice. , 2005, Cerebral cortex.

[19]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[20]  M. Just,et al.  Modifying the brain activation of poor readers during sentence comprehension with extended remedial instruction: A longitudinal study of neuroplasticity , 2008, Neuropsychologia.

[21]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[22]  S. Petersen,et al.  A developmental fMRI study of reading and repetition reveals changes in phonological and visual mechanisms over age. , 2008, Cerebral cortex.

[23]  A. B. Hollingshead,et al.  Four factor index of social status , 1975 .

[24]  Brian C. McKevitt,et al.  Best Practices in School Psychology IV , 1990 .

[25]  M. Just,et al.  From the Selectedworks of Marcel Adam Just Neural Basis of Dyslexia: a Comparison between Dyslexic and Non-dyslexic Children Equated for Reading Ability Neural Basis of Dyslexia: a Comparison between Dyslexic and Nondyslexic Children Equated for Reading Ability , 2022 .

[26]  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.

[27]  Andrés Martin,et al.  Overcoming Dyslexia: A New and Complete Science-Based Program for Reading Problems at Any Level , 2005 .

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

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

[30]  James R. Booth,et al.  Functional Anatomy of Intra- and Cross-Modal Lexical Tasks , 2002, NeuroImage.

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

[32]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[33]  Helen J. Neville,et al.  Maturational Constraints on the Recruitment of Early Processes for Syntactic Processing , 2011, Journal of Cognitive Neuroscience.

[34]  H. Neville,et al.  Language Acquisition and Cerebral Specialization in 20-Month-Old Infants , 1993, Journal of Cognitive Neuroscience.

[35]  D Bavelier,et al.  Cerebral organization for language in deaf and hearing subjects: biological constraints and effects of experience. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  K. James.  Sensori-motor experience leads to changes in visual processing in the developing brain. , 2010, Developmental science.

[37]  Gerald Matthews,et al.  Handbook of Individual Differences in Cognition , 2010 .

[38]  C. Blair,et al.  Relating effortful control, executive function, and false belief understanding to emerging math and literacy ability in kindergarten. , 2007, Child development.

[39]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[40]  R. Ivry,et al.  Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. , 2005, Journal of neurophysiology.

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

[42]  M. Posner,et al.  The Development of Executive Attention: Contributions to the Emergence of Self-Regulation , 2005, Developmental neuropsychology.

[43]  S Thesen,et al.  Prospective acquisition correction for head motion with image‐based tracking for real‐time fMRI , 2000, Magnetic resonance in medicine.

[44]  Barry Horwitz,et al.  A Functional Lesion in Developmental Dyslexia: Left Angular Gyral Blood Flow Predicts Severity , 1999, Brain and Language.

[45]  Carolyn A. Denton,et al.  Early development of neurophysiological processes involved in normal reading and reading disability: a magnetic source imaging study. , 2005, Neuropsychology.

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

[47]  H. Neville,et al.  Maturational Constraints on Functional Specializations for Language Processing: ERP and Behavioral Evidence in Bilingual Speakers , 1996, Journal of Cognitive Neuroscience.

[48]  Guinevere F. Eden,et al.  Attention to single letters activates left extrastriate cortex , 2004, NeuroImage.

[49]  E. Cabanis,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy and Mri , 1991 .

[50]  Ruth Fielding-Barnsley,et al.  Evaluation of a program to teach phonemic awareness to young children: A 2- and 3-year follow-up and a new preschool trial. , 1995 .

[51]  Megan M. McClelland,et al.  Children at risk for early academic problems: the role of learning-related social skills , 2000 .

[52]  Jack M Fletcher,et al.  Altering the brain circuits for reading through intervention: a magnetic source imaging study. , 2007, Neuropsychology.

[53]  Isabel Gauthier,et al.  Letter processing in the visual system: Different activation patterns for single letters and strings , 2005, Cognitive, affective & behavioral neuroscience.

[54]  M. Moreno.  School readiness. , 2013, JAMA pediatrics.

[55]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

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

[57]  S. Petersen,et al.  The effects of practice on the functional anatomy of task performance. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[59]  R. Poldrack,et al.  Disrupted neural responses to phonological and orthographic processing in dyslexic children: an fMRI study , 2001, Neuroreport.

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

[61]  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.

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

[63]  Thomas A Zeffiro,et al.  Development of neural mechanisms for reading , 2003, Nature Neuroscience.

[64]  Karen M. Jones,et al.  Neural Changes following Remediation in Adult Developmental Dyslexia , 2004, Neuron.

[65]  Beth A. Harn,et al.  Examining the Role of Attention and Instruction in At-Risk Kindergarteners , 2013, Journal of learning disabilities.

[66]  P. Skudlarski,et al.  Development of left occipitotemporal systems for skilled reading in children after a phonologically- based intervention , 2004, Biological Psychiatry.