Topological properties of large-scale structural brain networks in children with familial risk for reading difficulties

Developmental dyslexia is a neurobiological deficit characterized by persistent difficulty in learning to read in children and adults who otherwise possess normal intelligence. Functional and structural connectivity data suggest that developmental dyslexia could be a disconnection syndrome. However, whether abnormalities in connectivity exist in beginning readers at-risk for reading difficulties is unknown. Using graph-theoretical analysis, we investigated differences in global and regional topological properties of structural brain networks in 42 beginning readers with (FH+) and without (FH-) familial risk for reading difficulties. We constructed separate structural correlation networks based on measures of surface area and cortical thickness. Results revealed changes in topological properties in brain regions known to be abnormal in dyslexia (left supramarginal gyrus, left inferior frontal gyrus) in the FH+ group mainly in the network constructed from measures of cortical surface area. We also found alterations in topological properties in regions that are not often advertised as dyslexia but nonetheless play important role in reading (left posterior cingulate, hippocampus, and left precentral gyrus). To our knowledge, this is the first report of altered topological properties of structural correlation networks in children at risk for reading difficulty, and motivates future studies that examine the mechanisms underlying how these brain networks may mediate the influences of family history on reading outcome.

[1]  Yong He,et al.  Graph theoretical modeling of brain connectivity. , 2010, Current opinion in neurology.

[2]  M. Casanova,et al.  Magnetic Resonance Imaging Study of Brain Asymmetries in Dyslexic Patients , 2005, Journal of child neurology.

[3]  M. Beauchamp,et al.  Surface area accounts for the relation of gray matter volume to reading-related skills and history of dyslexia. , 2010, Cerebral cortex.

[4]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[5]  William B. Dobyns,et al.  G Protein-Coupled Receptor-Dependent Development of Human Frontal Cortex , 2004, Science.

[6]  A. Galaburda,et al.  Cerebrocortical microdysgenesis in neurologically normal subjects , 1989, Neurology.

[7]  E. Andermann,et al.  Genetics of the polymicrogyria syndromes , 2005, Journal of Medical Genetics.

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

[9]  Alan C. Evans,et al.  Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. , 2009, Cerebral cortex.

[10]  Karl J. Friston,et al.  Dissociating Reading Processes on the Basis of Neuronal Interactions , 2005, Journal of Cognitive Neuroscience.

[11]  Anders M. Dale,et al.  Sex-dependent association of common variants of microcephaly genes with brain structure , 2009, Proceedings of the National Academy of Sciences.

[12]  Charles Hulme,et al.  The Brain Basis of the Phonological Deficit in Dyslexia Is Independent of IQ , 2011, Psychological science.

[13]  Olaf Sporns,et al.  Weight-conserving characterization of complex functional brain networks , 2011, NeuroImage.

[14]  Gretel Sanabria-Diaz,et al.  Surface area and cortical thickness descriptors reveal different attributes of the structural human brain networks , 2010, NeuroImage.

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

[16]  A. Galaburda,et al.  Behavior, ectopias and immunity in BD/DB reciprocal crosses , 1992, Brain Research.

[17]  D. Simard,et al.  Fastest learning in small-world neural networks , 2004, physics/0402076.

[18]  E. T. Possing,et al.  Neural Correlates of Lexical Access during Visual Word Recognition , 2003, Journal of Cognitive Neuroscience.

[19]  U. Francke,et al.  Comparative study of brain morphology in Mecp2 mutant mouse models of Rett syndrome , 2008, The Journal of comparative neurology.

[20]  Jun Li,et al.  Brain Anatomical Network and Intelligence , 2009, NeuroImage.

[21]  Jean-Baptiste Poline,et al.  Genetic Variants of FOXP2 and KIAA0319/TTRAP/THEM2 Locus Are Associated with Altered Brain Activation in Distinct Language-Related Regions , 2012, The Journal of Neuroscience.

[22]  A. Dale,et al.  Distinct genetic influences on cortical surface area and cortical thickness. , 2009, Cerebral cortex.

[23]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[24]  Alan C. Evans,et al.  Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. , 2007, Cerebral cortex.

[25]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Petersen,et al.  A procedure for identifying regions preferentially activated by attention to semantic and phonological relations using functional magnetic resonance imaging , 2003, Neuropsychologia.

[27]  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.

[28]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[29]  M. Bornstein,et al.  Socioeconomic Status, Parenting, and Child Development , 2003 .

[30]  B. Franke,et al.  A theoretical molecular network for dyslexia: integrating available genetic findings , 2011, Molecular Psychiatry.

[31]  R. Plomin,et al.  Parent-offspring resemblance for reading performance at 7, 12 and 16 years of age in the Colorado Adoption Project. , 2002, Journal of child psychology and psychiatry, and allied disciplines.

[32]  Elena L. Grigorenko,et al.  Same or different? Insights into the etiology of phonological awareness and rapid naming , 2009, Biological Psychology.

[33]  Alan C. Evans,et al.  Structural Insights into Aberrant Topological Patterns of Large-Scale Cortical Networks in Alzheimer's Disease , 2008, The Journal of Neuroscience.

[34]  S M Hadi Hosseini,et al.  Altered small-world properties of gray matter networks in breast cancer , 2012, BMC Neurology.

[35]  E. L. Berry,et al.  Association of abnormal cerebellar activation with motor learning difficulties in dyslexic adults , 1999, The Lancet.

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

[37]  Hans-Ulrich Dodt,et al.  Ultramicroscopy – Imaging a Whole Animal or a Whole Brain with Micron Resolution , 2011, Front. Neurosci..

[38]  A. Dale,et al.  Regional and progressive thinning of the cortical ribbon in Huntington’s disease , 2002, Neurology.

[39]  J. Fiez,et al.  Impact of Cerebellar Lesions on Reading and Phonological Processing , 2008, Annals of the New York Academy of Sciences.

[40]  Emily A. Farris,et al.  Brain connectivity in non-reading impaired children and children diagnosed with developmental dyslexia , 2009, Neuropsychologia.

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

[42]  Tilo Kircher,et al.  Neural correlates of narrative shifts during auditory story comprehension , 2009, NeuroImage.

[43]  T. Sejnowski,et al.  A universal scaling law between gray matter and white matter of cerebral cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Sang Won Seo,et al.  Sulcal morphology changes and their relationship with cortical thickness and gyral white matter volume in mild cognitive impairment and Alzheimer's disease , 2008, NeuroImage.

[45]  A. Levey,et al.  Alterations in Cortical Thickness and White Matter Integrity in Mild Cognitive Impairment Measured by Whole-Brain Cortical Thickness Mapping and Diffusion Tensor Imaging , 2009, American Journal of Neuroradiology.

[46]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[47]  Heikki Lyytinen,et al.  Maternal history of reading difficulty is associated with reduced language-related gray matter in beginning readers , 2012, NeuroImage.

[48]  A. Baddeley Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

[49]  Marcus Kaiser,et al.  Nonoptimal Component Placement, but Short Processing Paths, due to Long-Distance Projections in Neural Systems , 2006, PLoS Comput. Biol..

[50]  Richard E. Frye,et al.  Greater Pre-Stimulus Effective Connectivity from the Left Inferior Frontal Area to other Areas is Associated with Better Phonological Decoding in Dyslexic Readers , 2010, Front. Syst. Neurosci..

[51]  L. Petrosini,et al.  Do children with developmental dyslexia have an implicit learning deficit? , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[52]  M. Segawa,et al.  Development of language in Rett syndrome , 2001, Brain and Development.

[53]  J. Fletcher,et al.  Neural correlates of sentence reading in children with reading difficulties , 2011, Neuroreport.

[54]  Jack M Fletcher,et al.  Brain Mechanisms for Reading in Children With and Without Dyslexia: A Review of Studies of Normal Development and Plasticity , 2003, Developmental neuropsychology.

[55]  Alan C. Evans,et al.  Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI , 2006, NeuroImage.

[56]  Alan C. Evans,et al.  Revealing modular architecture of human brain structural networks by using cortical thickness from MRI. , 2008, Cerebral cortex.

[57]  Anders M. Dale,et al.  Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer , 2006, NeuroImage.

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

[59]  H. Johansen-Berg,et al.  Maternal antibody-mediated dyslexia? Evidence for a pathogenic serum factor in a mother of two dyslexic children shown by transfer to mice using behavioural studies and magnetic resonance spectroscopy , 2002, Journal of Neuroimmunology.

[60]  Manuel Carreiras,et al.  Brain Activation for Lexical Decision and Reading Aloud: Two Sides of the Same Coin? , 2007, Journal of Cognitive Neuroscience.

[61]  C. Papageorgiou,et al.  Evidence of a posterior cingulate involvement (Brodmann area 31) in dyslexia: A study based on source localization algorithm of event-related potentials , 2008, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[62]  Andreas Daffertshofer,et al.  Comparing Brain Networks of Different Size and Connectivity Density Using Graph Theory , 2010, PloS one.

[63]  Riitta Hari,et al.  Human ROBO1 Regulates Interaural Interaction in Auditory Pathways , 2012, The Journal of Neuroscience.

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

[65]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[66]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[67]  Bruce Fischl,et al.  Geometrically Accurate Topology-Correction of Cortical Surfaces Using Nonseparating Loops , 2007, IEEE Transactions on Medical Imaging.

[68]  Boris C. Bernhardt,et al.  Mapping limbic network organization in temporal lobe epilepsy using morphometric correlations: Insights on the relation between mesiotemporal connectivity and cortical atrophy , 2008, NeuroImage.

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

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

[71]  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.

[72]  Jong-Min Lee,et al.  Cortical thickness in single- versus multiple-domain amnestic mild cognitive impairment , 2007, NeuroImage.

[73]  Vince D. Calhoun,et al.  Polymorphism of DCDC2 Reveals Differences in Cortical Morphology of Healthy Individuals—A Preliminary Voxel Based Morphometry Study , 2008, Brain Imaging and Behavior.

[74]  K. Worsley,et al.  Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load. , 2009, Brain : a journal of neurology.

[75]  D. Pauls,et al.  The genetics of reading disability , 2009, Current psychiatry reports.

[76]  Elena L. Grigorenko,et al.  Genetic bases of developmental dyslexia: A capsule review of heritability estimates , 2004 .

[77]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[78]  Thomas E. Nichols,et al.  Controlling the familywise error rate in functional neuroimaging: a comparative review , 2003, Statistical methods in medical research.

[79]  A. Galaburda,et al.  Effects of the autoimmune uterine/maternal environment upon cortical ectopias, behavior and autoimmunity , 1991, Brain Research.

[80]  K. Hasan,et al.  Diffusion tensor quantification of the relations between microstructural and macrostructural indices of white matter and reading , 2011, Human brain mapping.

[81]  A. Dale,et al.  Thinning of the cerebral cortex in aging. , 2004, Cerebral cortex.

[82]  K. Eklund,et al.  Parental literacy predicts children's literacy: a longitudinal family-risk study. , 2011, Dyslexia.

[83]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[84]  R. Tsien,et al.  Specificity and Stability in Topology of Protein Networks , 2022 .

[85]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[86]  Yu Wang,et al.  Disruption of neuronal migration by RNAi of Dyx1c1 results in neocortical and hippocampal malformations. , 2007, Cerebral cortex.

[87]  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.

[88]  Marianna D. Eddy,et al.  Regionally localized thinning of the cerebral cortex in schizophrenia , 2003, Schizophrenia Research.

[89]  Dinggang Shen,et al.  Brain anatomical networks in early human brain development , 2011, NeuroImage.

[90]  Anders M. Dale,et al.  A hybrid approach to the Skull Stripping problem in MRI , 2001, NeuroImage.

[91]  J. Hajnal,et al.  Abnormal Cortical Development after Premature Birth Shown by Altered Allometric Scaling of Brain Growth , 2006, PLoS medicine.

[92]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

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

[94]  J. Ziegler,et al.  Reading acquisition, developmental dyslexia, and skilled reading across languages: a psycholinguistic grain size theory. , 2005, Psychological bulletin.

[95]  R. Kahn,et al.  Efficiency of Functional Brain Networks and Intellectual Performance , 2009, The Journal of Neuroscience.

[96]  Ulla Richardson,et al.  Print-specific multimodal brain activation in kindergarten improves prediction of reading skills in second grade , 2011, NeuroImage.

[97]  Xi-Nian Zuo,et al.  Resting-State Functional Connectivity Indexes Reading Competence in Children and Adults , 2011, The Journal of Neuroscience.

[98]  A. Riecker,et al.  The contribution of white and gray matter differences to developmental dyslexia: Insights from DTI and VBM at 3.0T , 2008, Neuropsychologia.

[99]  Philip D. Harvey,et al.  Dysregulation of X‐linked gene expression in Klinefelter's syndrome and association with verbal cognition , 2007, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[100]  S Eliez,et al.  Morphological alteration of temporal lobe gray matter in dyslexia: an MRI study. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[101]  Vincent J Schmithorst,et al.  Comparison of fMRI data from passive listening and active‐response story processing tasks in children , 2009, Journal of magnetic resonance imaging : JMRI.

[102]  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.

[103]  Walter Schneider,et al.  Identifying the brain's most globally connected regions , 2010, NeuroImage.

[104]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[105]  Nadine Gaab,et al.  Functional characteristics of developmental dyslexia in left-hemispheric posterior brain regions predate reading onset , 2012, Proceedings of the National Academy of Sciences.

[106]  Anders M. Dale,et al.  Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex , 2001, IEEE Transactions on Medical Imaging.

[107]  Heikki Lyytinen,et al.  Early Identification and Prevention of Dyslexia: Results from a Prospective Follow-up Study of Children at Familial Risk for Dyslexia , 2008 .

[108]  J. Gabrieli,et al.  Functional and morphometric brain dissociation between dyslexia and reading ability , 2007, Proceedings of the National Academy of Sciences.

[109]  Edward H Herskovits,et al.  Neural regions essential for reading and spelling of words and pseudowords , 2007, Annals of neurology.

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

[111]  Robert H. Bradley,et al.  Home observation for measurement of the environment , 1979 .

[112]  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.

[113]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[114]  B. L. Miller,et al.  Reading disorders in primary progressive aphasia: A behavioral and neuroimaging study , 2009, Neuropsychologia.

[115]  B. Horwitz,et al.  Functional connectivity of the angular gyrus in normal reading and dyslexia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[116]  W. Kaufmann,et al.  Early progressive encephalopathy in boys and MECP2 mutations , 2006, Neurology.

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

[118]  Heikki Lyytinen,et al.  Trajectories of Reading Development: A Follow-up From Birth to School Age of Children With and Without Risk for Dyslexia , 2006 .

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

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

[121]  A. van der Leij,et al.  Child and parental literacy levels within families with a history of dyslexia. , 2012, Journal of child psychology and psychiatry, and allied disciplines.

[122]  Joanna A. Christodoulou,et al.  Brain basis of phonological awareness for spoken language in children and its disruption in dyslexia. , 2012, Cerebral cortex.

[123]  Ingrid Agartz,et al.  A common MECP2 haplotype associates with reduced cortical surface area in humans in two independent populations , 2009, Proceedings of the National Academy of Sciences.

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

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

[126]  M. Habib,et al.  The neurological basis of developmental dyslexia: an overview and working hypothesis. , 2000, Brain : a journal of neurology.

[127]  Jenifer Juranek,et al.  Functional disruption of the brain mechanism for reading: effects of comorbidity and task difficulty among children with developmental learning problems. , 2011, Neuropsychology.

[128]  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 .

[129]  Fumiko Hoeft,et al.  GAT: A Graph-Theoretical Analysis Toolbox for Analyzing Between-Group Differences in Large-Scale Structural and Functional Brain Networks , 2012, PloS one.

[130]  N. Craddock,et al.  MECP2 structural and 3′‐UTR variants in schizophrenia, autism and other psychiatric diseases: A possible association with autism , 2004, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[131]  Neda Bernasconi,et al.  Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. , 2011, Cerebral cortex.

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

[133]  Karl J. Friston,et al.  Supra-regional brain systems and the neuropathology of schizophrenia. , 1999, Cerebral cortex.

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

[135]  A. Dale,et al.  Improved Localizadon of Cortical Activity by Combining EEG and MEG with MRI Cortical Surface Reconstruction: A Linear Approach , 1993, Journal of Cognitive Neuroscience.

[136]  J. Cheverud,et al.  Quantitative genetics and developmental constraints on evolution by selection. , 1984, Journal of theoretical biology.

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

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

[139]  E. Bullmore,et al.  Hierarchical Organization of Human Cortical Networks in Health and Schizophrenia , 2008, The Journal of Neuroscience.

[140]  Bernard Mazoyer,et al.  Word and non-word reading: What role for the Visual Word Form Area? , 2005, NeuroImage.

[141]  B. Dickerson,et al.  Age-Related Changes in the Thickness of Cortical Zones in Humans , 2011, Brain Topography.

[142]  L. Katz,et al.  Lexical decision as an endophenotype for reading comprehension: An exploration of an association , 2012, Development and Psychopathology.

[143]  Bruce Fischl,et al.  Genetic and environmental contributions to regional cortical surface area in humans: a magnetic resonance imaging twin study. , 2011, Cerebral cortex.

[144]  Anders M. Dale,et al.  Sequence-independent segmentation of magnetic resonance images , 2004, NeuroImage.

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