Brain white matter structure and language ability in preschool-aged children

HighlightsWe tested how pre‐reading language relates to brain structure in children 3–5 years.Phonological processing was related to diffusion parameters in ventral white matter.We also observe relationships in non‐traditional reading areas.Results show that brain alterations predate reading instruction. ABSTRACT Brain alterations are associated with reading and language difficulties in older children, but little research has investigated relationships between early language skills and brain white matter structure during the preschool period. We studied 68 children aged 3.0–5.6 years who underwent diffusion tensor imaging and participated in assessments of Phonological Processing and Speeded Naming. Tract‐based spatial statistics and tractography revealed relationships between Phonological Processing and diffusion parameters in bilateral ventral white matter pathways and the corpus callosum. Phonological Processing was positively correlated with fractional anisotropy and negatively correlated with mean diffusivity. The relationships observed in left ventral pathways are consistent with studies in older children, and demonstrate that structural markers for language performance are apparent as young as 3 years of age. Our findings in right hemisphere areas that are not as commonly found in adult studies suggest that young children rely on a widespread network for language processing that becomes more specialized with age.

[1]  L. Mccargar,et al.  The Alberta Pregnancy Outcomes and Nutrition (APrON) cohort study: rationale and methods. , 2014, Maternal & child nutrition.

[2]  M. Smits,et al.  White matter tracts of speech and language. , 2014, Seminars in ultrasound, CT, and MR.

[3]  Shu-Wei Sun,et al.  Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia , 2003, NeuroImage.

[4]  S. Deoni,et al.  Interactions between White Matter Asymmetry and Language during Neurodevelopment , 2013, The Journal of Neuroscience.

[5]  W. Lutzenberger,et al.  Increases in language lateralization in normal children as observed using magnetoencephalography , 2008, Brain and Language.

[6]  David E. Osher,et al.  Tracking the Roots of Reading Ability: White Matter Volume and Integrity Correlate with Phonological Awareness in Prereading and Early-Reading Kindergarten Children , 2013, The Journal of Neuroscience.

[7]  Torsten Baldeweg,et al.  Maturation of language networks in children: A systematic review of 22years of functional MRI , 2015, NeuroImage.

[8]  T. Klingberg,et al.  Maturation of White Matter is Associated with the Development of Cognitive Functions during Childhood , 2004, Journal of Cognitive Neuroscience.

[9]  Aad van der Lugt,et al.  Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: A combined fMRI and DTI study , 2007, NeuroImage.

[10]  Brian T. Gold,et al.  Speed of lexical decision correlates with diffusion anisotropy in left parietal and frontal white matter: Evidence from diffusion tensor imaging , 2007, Neuropsychologia.

[11]  J. Gabrieli.  Dyslexia: A New Synergy Between Education and Cognitive Neuroscience , 2009, Science.

[12]  Heidi Johansen-Berg,et al.  Changes in white matter microstructure during adolescence , 2008, NeuroImage.

[13]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[14]  Julia M. Carroll,et al.  Literacy difficulties and psychiatric disorders: evidence for comorbidity. , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[15]  Hangyi Jiang,et al.  Pediatric diffusion tensor imaging: Normal database and observation of the white matter maturation in early childhood , 2006, NeuroImage.

[16]  Bruce D. McCandliss,et al.  Left lateralized white matter microstructure accounts for individual differences in reading ability and disability , 2006, Neuropsychologia.

[17]  O. Sporns,et al.  White matter maturation reshapes structural connectivity in the late developing human brain , 2010, Proceedings of the National Academy of Sciences.

[18]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[19]  B. Wandell,et al.  Development of white matter and reading skills , 2012, Proceedings of the National Academy of Sciences.

[20]  Margot J. Taylor,et al.  Characterizing the Normal Developmental Trajectory of Expressive Language Lateralization Using Magnetoencephalography , 2011, Journal of the International Neuropsychological Society.

[21]  C. Lebel,et al.  Lateralization of the arcuate fasciculus from childhood to adulthood and its relation to cognitive abilities in children , 2009, Human brain mapping.

[22]  Angela D. Friederici,et al.  Maturation of the Language Network: From Inter- to Intrahemispheric Connectivities , 2011, PloS one.

[23]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[24]  Matthew P. G. Allin,et al.  Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography , 2011, NeuroImage.

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

[26]  Ke Zhou,et al.  Diffusion tensor imaging of normal white matter maturation from late childhood to young adulthood: Voxel-wise evaluation of mean diffusivity, fractional anisotropy, radial and axial diffusivities, and correlation with reading development , 2008, NeuroImage.

[27]  Brian A. Wandell,et al.  Anatomical Properties of the Arcuate Fasciculus Predict Phonological and Reading Skills in Children , 2011, Journal of Cognitive Neuroscience.

[28]  Richard E. Frye,et al.  Splenium microstructure is related to two dimensions of reading skill , 2008, Neuroreport.

[29]  Marit Korkman,et al.  NEPSY II: clinical and interpretive manual , 2007 .

[30]  J. Wouters,et al.  A tractography study in dyslexia: neuroanatomic correlates of orthographic, phonological and speech processing. , 2012, Brain : a journal of neurology.

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

[32]  Luis Concha,et al.  Imaging brain connectivity in children with diverse reading ability , 2005, NeuroImage.

[33]  F. Colle,et al.  Therapeutic patient education for stroke survivors: Non-pharmacological management. A literature review. , 2012, Annals of physical and rehabilitation medicine.

[34]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[35]  T. Klingberg.  Microstructure of temporo-parietal white matter as a basis for reading ability: evidence from DTI , 2002, European Psychiatry.

[36]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

[37]  Pascale Tremblay,et al.  Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. , 2012, Brain : a journal of neurology.

[38]  Eric A. Roy,et al.  A Performance Measure of the Degree of Hand Preference , 2000, Brain and Cognition.

[39]  Alexander Leemans,et al.  Microstructural maturation of the human brain from childhood to adulthood , 2008, NeuroImage.

[40]  C. Lebel,et al.  Longitudinal Development of Human Brain Wiring Continues from Childhood into Adulthood , 2011, The Journal of Neuroscience.

[41]  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.

[42]  Alfred Anwander,et al.  Neuroanatomical prerequisites for language functions in the maturing brain. , 2011, Cerebral cortex.

[43]  M. Just,et al.  Altering Cortical Connectivity: Remediation-Induced Changes in the White Matter of Poor Readers , 2009, Neuron.

[44]  Jesper Andersson,et al.  Changes in white matter microstructure in the developing brain—A longitudinal diffusion tensor imaging study of children from 4 to 11 years of age , 2016, NeuroImage.

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

[46]  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.

[47]  T. Whitlock.  Dyslexia , 1989, The Lancet.

[48]  Jan Wouters,et al.  A DTI tractography study in pre-readers at risk for dyslexia , 2015, Developmental Cognitive Neuroscience.

[49]  C. Elbro,et al.  Long-Term Effects of Phoneme Awareness and Letter Sound Training: An Intervention Study With Children at Risk for Dyslexia. , 2004 .

[50]  Pek-Lan Khong,et al.  Lateralization of the arcuate fasciculus and its differential correlation with reading ability between young learners and experienced readers: A diffusion tensor tractography study in a chinese cohort , 2011, Human brain mapping.

[51]  Sally Shaywitz,et al.  Diffusion tensor imaging correlates of reading ability in dysfluent and non-impaired readers , 2013, Brain and Language.

[52]  B. Wandell,et al.  Children's Reading Performance is Correlated with White Matter Structure Measured by Diffusion Tensor Imaging , 2005, Cortex.

[53]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[54]  P. Batchelor,et al.  International Society for Magnetic Resonance in Medicine , 1997 .

[55]  Michel Thiebaut de Schotten,et al.  Short frontal lobe connections of the human brain , 2012, Cortex.

[56]  Helen J. Neville,et al.  Emergence of the neural network for reading in five-year-old beginning readers of different levels of pre-literacy abilities: An fMRI study , 2011, NeuroImage.

[57]  N. Gaab,et al.  Development of Tract‐Specific White Matter Pathways During Early Reading Development in At‐Risk Children and Typical Controls , 2016, Cerebral cortex.

[58]  Brian A Wandell,et al.  Temporal-callosal pathway diffusivity predicts phonological skills in children , 2007, Proceedings of the National Academy of Sciences.

[59]  J. Wouters,et al.  Neuroscience and Biobehavioral Reviews a Qualitative and Quantitative Review of Diffusion Tensor Imaging Studies in Reading and Dyslexia , 2022 .

[60]  John Russell,et al.  Dysmyelination Revealed through MRI as Increased Radial (but Unchanged Axial) Diffusion of Water , 2002, NeuroImage.

[61]  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.

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

[63]  Pascale Tremblay,et al.  Fiber tracking of the frontal aslant tract and subcomponents of the arcuate fasciculus in 5–8-year-olds: Relation to speech and language function , 2015, Brain and Language.

[64]  Nicolas Langer,et al.  White Matter Alterations in Infants at Risk for Developmental Dyslexia , 2015, Cerebral cortex.

[65]  Laurie E. Cutting,et al.  White matter microstructural differences linked to left perisylvian language network in children with dyslexia , 2010, Cortex.

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

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

[68]  Cedric E. Ginestet,et al.  White matter development and early cognition in babies and toddlers , 2014, Human brain mapping.