Resting-State Functional Connectivity Indexes Reading Competence in Children and Adults

Task-based neuroimaging studies face the challenge of developing tasks capable of equivalently probing reading networks across different age groups. Resting-state fMRI, which requires no specific task, circumvents these difficulties. Here, in 25 children (8–14 years) and 25 adults (21–46 years), we examined the extent to which individual differences in reading competence can be related to resting-state functional connectivity (RSFC) of regions implicated in reading. In both age groups, reading standard scores correlated positively with RSFC between the left precentral gyrus and other motor regions, and between Broca's and Wernicke's areas. This suggests that, regardless of age group, stronger coupling among motor regions, as well as between language/speech regions, subserves better reading, presumably reflecting automatized articulation. We also observed divergent RSFC–behavior relationships in children and adults, particularly those anchored in the left fusiform gyrus (FFG) (the visual word form area). In adults, but not children, better reading performance was associated with stronger positive correlations between FFG and phonology-related regions (Broca's area and the left inferior parietal lobule), and with stronger negative relationships between FFG and regions of the “task-negative” default network. These results suggest that both positive RSFC (functional coupling) between reading regions and negative RSFC (functional segregation) between a reading region and default network regions are important for automatized reading, characteristic of adult readers. Together, our task-independent RSFC findings highlight the importance of appreciating developmental changes in the neural correlates of reading competence, and suggest that RSFC may serve to facilitate the identification of reading disorders in different age groups.

[1]  M. Catani,et al.  The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state , 2008, Cortex.

[2]  Friedemann Pulvermüller,et al.  Motor cortex maps articulatory features of speech sounds , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Jonathan D. Power,et al.  The Development of Human Functional Brain Networks , 2010, Neuron.

[4]  James R. Booth,et al.  Developmental changes in activation and effective connectivity in phonological processing , 2007, NeuroImage.

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

[6]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[7]  U. Goswami,et al.  Rhythmic processing in children with developmental dyslexia: Auditory and motor rhythms link to reading and spelling , 2008, Journal of Physiology-Paris.

[8]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[9]  S. Dehaene,et al.  The visual word form area: a prelexical representation of visual words in the fusiform gyrus , 2002, Neuroreport.

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

[11]  Joseph T. Devlin,et al.  Supramarginal gyrus involvement in visual word recognition , 2009, Cortex.

[12]  Abraham Z. Snyder,et al.  Maturing Thalamocortical Functional Connectivity Across Development , 2010, Front. Syst. Neurosci..

[13]  Michael P Milham,et al.  Reading networks at rest. , 2010, Cerebral cortex.

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

[15]  Bradley L Schlaggar,et al.  Functional Neuroimaging Insights Into the Development of Skilled Reading , 2009, Current directions in psychological science.

[16]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[18]  M. Roth,et al.  Premotor activations in response to visually presented single letters depend on the hand used to write: a study on left-handers , 2005, Neuropsychologia.

[19]  A M Liberman,et al.  Perception of the speech code. , 1967, Psychological review.

[20]  Tim Fosker,et al.  Language-universal Sensory Deficits in Developmental Dyslexia: English, Spanish, and Chinese , 2011, Journal of Cognitive Neuroscience.

[21]  J. Jameson,et al.  SF1 in the Development of the Adrenal Gland and Gonads , 2003, Hormone Research in Paediatrics.

[22]  Emilio Ferrer,et al.  Uncoupling of Reading and IQ Over Time , 2010, Psychological science.

[23]  L. Uddin,et al.  Functional Brain Correlates of Social and Nonsocial Processes in Autism Spectrum Disorders: An Activation Likelihood Estimation Meta-Analysis , 2009, Biological Psychiatry.

[24]  S. Gathercole,et al.  Working memory in children with reading disabilities. , 2006, Journal of experimental child psychology.

[25]  Akram Bakkour,et al.  Intrinsic interhemispheric hippocampal functional connectivity predicts individual differences in memory performance ability , 2010, Hippocampus.

[26]  Jonathan D. Power,et al.  Functional Brain Networks Develop from a “Local to Distributed” Organization , 2009, PLoS Comput. Biol..

[27]  G. Eden,et al.  Development of Ventral Stream Representations for Single Letters , 2008, Annals of the New York Academy of Sciences.

[28]  Kaustubh Supekar,et al.  Development of Large-Scale Functional Brain Networks in Children , 2009, NeuroImage.

[29]  Marco Iacoboni,et al.  The Essential Role of Premotor Cortex in Speech Perception , 2007, Current Biology.

[30]  D. Margulies,et al.  Development of anterior cingulate functional connectivity from late childhood to early adulthood. , 2009, Cerebral cortex.

[31]  Marc Joliot,et al.  Mapping numerical processing, reading, and executive functions in the developing brain: an fMRI meta-analysis of 52 studies including 842 children. , 2010, Developmental science.

[32]  Laurie S. Glezer,et al.  Evidence for Highly Selective Neuronal Tuning to Whole Words in the “Visual Word Form Area” , 2009, Neuron.

[33]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[34]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[35]  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.

[36]  T. Paus,et al.  Functional coactivation map of the human brain. , 2008, Cerebral cortex.

[37]  B. Pennington,et al.  Sensory processing, reading, IQ, and attention. , 2004, Journal of experimental child psychology.

[38]  Bharat B. Biswal,et al.  Competition between functional brain networks mediates behavioral variability , 2008, NeuroImage.

[39]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[40]  James R. Booth,et al.  Developmental increases in effective connectivity to brain regions involved in phonological processing during tasks with orthographic demands , 2008, Brain Research.

[41]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[42]  K. Grieve,et al.  The primate pulvinar nuclei: vision and action , 2000, Trends in Neurosciences.

[43]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[44]  N. Geschwind.  Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

[45]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[46]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[47]  Christine L. Cox,et al.  Your Resting Brain CAREs about Your Risky Behavior , 2010, PloS one.

[48]  Alan C. Evans,et al.  Growing Together and Growing Apart: Regional and Sex Differences in the Lifespan Developmental Trajectories of Functional Homotopy , 2010, The Journal of Neuroscience.

[49]  Michael D. Greicius,et al.  Development of functional and structural connectivity within the default mode network in young children , 2010, NeuroImage.

[50]  N. Ryan,et al.  Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[51]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[52]  L. Fadiga,et al.  Active perception: sensorimotor circuits as a cortical basis for language , 2010, Nature Reviews Neuroscience.

[53]  G Mann,et al.  ON THE THALAMUS * , 1905, British medical journal.

[54]  Jin Fan,et al.  The activation of attentional networks , 2005, NeuroImage.

[55]  M. Jenkinson.  Non-linear registration aka Spatial normalisation , 2007 .

[56]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[57]  W. Schneider,et al.  Cross‐cultural effect on the brain revisited: Universal structures plus writing system variation , 2005, Human brain mapping.

[58]  Jonathan D. Power,et al.  Prediction of Individual Brain Maturity Using fMRI , 2010, Science.

[59]  W D Gaillard,et al.  fMRI identifies regional specialization of neural networks for reading in young children , 2003, Neurology.

[60]  Trichur Raman Vidyasagar.  A neuronal model of attentional spotlight: parietal guiding the temporal , 1999, Brain Research Reviews.

[61]  Michelle Hampson,et al.  Connectivity–behavior analysis reveals that functional connectivity between left BA39 and Broca's area varies with reading ability , 2006, NeuroImage.

[62]  C. McBride-Chang,et al.  Models of speech perception and phonological processing in reading. , 1996, Child development.

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

[64]  S. Petersen,et al.  The “Task B problem” and other considerations in developmental functional neuroimaging , 2010, Human brain mapping.

[65]  M. Petrides,et al.  Broca’s region: linking human brain functional connectivity data and non‐human primate tracing anatomy studies , 2010, The European journal of neuroscience.

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