White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study.

Maturation of brain white matter pathways is an important factor in cognitive, behavioral, emotional and motor development during childhood and adolescence. In this study, we investigate white matter maturation as reflected by changes in anisotropy and white matter density with age. Thirty-four children and adolescents aged 6-19 years received diffusion-weighted magnetic resonance imaging scans. Among these, 30 children and adolescents also received high-resolution T1-weighed anatomical scans. A linear regression model was used to correlate fractional anisotropy (FA) values with age on a voxel-by-voxel basis. Within the regions that showed significant FA changes with age, a post hoc analysis was performed to investigate white matter density changes. With increasing age, FA values increased in prefrontal regions, in the internal capsule as well as in basal ganglia and thalamic pathways, the ventral visual pathways, and the corpus callosum. The posterior limb of the internal capsule, intrathalamic connections, and the corpus callosum showed the most significant overlaps between white matter density and FA changes with age. This study demonstrates that during childhood and adolescence, white matter anisotropy changes in brain regions that are important for attention, motor skills, cognitive ability, and memory. This typical developmental trajectory may be altered in individuals with disorders of development, cognition and behavior.

[1]  A. Minkowski,et al.  Regional Development of the Brain in Early Life , 1968 .

[2]  P. Huttenlocher Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[3]  D. Weinberger,et al.  Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence. , 1986, Archives of general psychiatry.

[4]  W. Greenough,et al.  Experience and brain development. , 1987, Child development.

[5]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[6]  D. Norman,et al.  Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. , 1988, Radiology.

[7]  T. Achenbach Manual for the child behavior checklist/4-18 and 1991 profile , 1991 .

[8]  Michal Neeman,et al.  A simple method for obtaining cross‐term‐free images for diffusion anisotropy studies in NMR microimaging , 1991, Magnetic resonance in medicine.

[9]  J. Kucharczyk,et al.  Magnetic resonance imaging of diffusion and perfusion , 1991, Topics in magnetic resonance imaging : TMRI.

[10]  Sohee Park,et al.  Schizophrenics show spatial working memory deficits. , 1992, Archives of general psychiatry.

[11]  C. Njiokiktjien,et al.  Callosal size in children with learning disabilities , 1994, Behavioural Brain Research.

[12]  D. Mathalon,et al.  A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. , 1994, Archives of neurology.

[13]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[14]  F. Benes,et al.  Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. , 1994, Archives of general psychiatry.

[15]  D. Friedman,et al.  The development of selective attention as reflected by event-related brain potentials. , 1995, Journal of experimental child psychology.

[16]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[17]  P. Basser,et al.  Toward a quantitative assessment of diffusion anisotropy , 1996, Magnetic resonance in medicine.

[18]  A. Reiss,et al.  Brain development, gender and IQ in children. A volumetric imaging study. , 1996, Brain : a journal of neurology.

[19]  W E Reddick,et al.  Age-related changes in the pediatric brain: quantitative MR evidence of maturational changes during adolescence. , 1997, AJNR. American journal of neuroradiology.

[20]  Karl J. Friston,et al.  Combining Spatial Extent and Peak Intensity to Test for Activations in Functional Imaging , 1997, NeuroImage.

[21]  Jonathan D. Cohen,et al.  A Developmental Functional MRI Study of Prefrontal Activation during Performance of a Go-No-Go Task , 1997, Journal of Cognitive Neuroscience.

[22]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[23]  C. Nelson,et al.  The functional emergence of prefrontally-guided working memory systems in four- to eight-year-old children , 1998, Neuropsychologia.

[24]  P. Maruff,et al.  Neuropsychological deficits in obsessive-compulsive disorder: a comparison with unipolar depression, panic disorder, and normal controls. , 1998, Archives of general psychiatry.

[25]  J. Cummings Frontal-subcortical circuits and human behavior. , 1993, Journal of psychosomatic research.

[26]  M. Thase,et al.  Prefrontal cortical dysfunction in depression determined by Wisconsin Card Sorting Test performance. , 1999, The American journal of psychiatry.

[27]  A. Toga,et al.  In vivo evidence for post-adolescent brain maturation in frontal and striatal regions , 1999, Nature Neuroscience.

[28]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[29]  I. Kovács,et al.  Late maturation of visual spatial integration in humans. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Alan C. Evans,et al.  Structural maturation of neural pathways in children and adolescents: in vivo study. , 1999, Science.

[31]  M. Jeeves,et al.  Bilateral field advantage and evoked potential interhemispheric transmission in commissurotomy and callosal agenesis , 1999, Neuropsychologia.

[32]  J. Gabrieli,et al.  Myelination and organization of the frontal white matter in children: a diffusion tensor MRI study. , 1999, Neuroreport.

[33]  Jagath C. Rajapakse,et al.  Development of the human corpus callosum during childhood and adolescence: A longitudinal MRI study , 1999, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[34]  Michael S. Gazzaniga,et al.  Direction information coordinated via the posterior third of the corpus callosum during bimanual movements , 1999, Experimental Brain Research.

[35]  J. Cohen,et al.  Context-processing deficits in schizophrenia: converging evidence from three theoretically motivated cognitive tasks. , 1999, Journal of abnormal psychology.

[36]  M. Keshavan,et al.  Corpus callosal signal intensity in treatment-naive pediatric obsessive compulsive disorders , 1999, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[37]  I. Kovács Human development of perceptual organization , 2000, Vision Research.

[38]  B. J. Casey,et al.  Structural and functional brain development and its relation to cognitive development , 2000, Biological Psychology.

[39]  Joaquín M. Fuster,et al.  Executive frontal functions , 2000, Experimental Brain Research.

[40]  D. Delis,et al.  Improved memory functioning and frontal lobe maturation between childhood and adolescence: A structural MRI study , 2001, Journal of the International Neuropsychological Society.

[41]  N. Minshew,et al.  Maturation of Widely Distributed Brain Function Subserves Cognitive Development , 2001, NeuroImage.

[42]  D. Bowers,et al.  Verbal Encoding Deficits in a Patient with a Left Retrosplenial Lesion , 2001, Neurocase.

[43]  G J Barker,et al.  Neuropathological abnormalities in schizophrenia: evidence from magnetization transfer imaging. , 2001, Brain : a journal of neurology.

[44]  C. Caltagirone,et al.  Interhemispheric transfer time in a patient with a partial lesion of the corpus callosum , 2001, Neuroreport.

[45]  Alan C. Evans,et al.  Maturation of white matter in the human brain: a review of magnetic resonance studies , 2001, Brain Research Bulletin.

[46]  J. Shimony,et al.  Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor MR imaging. , 2001, Radiology.

[47]  Fred L. Bookstein,et al.  Corpus Callosum Shape and Neuropsychological Deficits in Adult Males with Heavy Fetal Alcohol Exposure , 2002, NeuroImage.

[48]  V. Menon,et al.  Neural basis of protracted developmental changes in visuo-spatial working memory , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  M. Herrero,et al.  Functional anatomy of thalamus and basal ganglia , 2002, Child’s Nervous System.

[50]  Daphne Bavelier,et al.  Human brain plasticity: evidence from sensory deprivation and altered language experience. , 2002, Progress in brain research.

[51]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[52]  Dominique Hasboun,et al.  Relationship between attentional performance and corpus callosum morphometry in patients with Alzheimer’s disease , 2002, Neuropsychologia.

[53]  G. Logan,et al.  The Development of Selective Inhibitory Control Across the Life Span , 2002, Developmental neuropsychology.

[54]  Judy Reilly,et al.  Cognitive efficiency on a match to sample task decreases at the onset of puberty in children , 2002, Brain and Cognition.

[55]  A. Uluğ,et al.  Monitoring brain development with quantitative diffusion tensor imaging , 2002 .

[56]  J. Provenzale,et al.  Evaluation of normal age-related changes in anisotropy during infancy and childhood as shown by diffusion tensor imaging. , 2002, AJR. American journal of roentgenology.

[57]  V. Menon,et al.  Maturation of brain function associated with response inhibition. , 2002, Journal of the American Academy of Child and Adolescent Psychiatry.

[58]  A. Quittner,et al.  Behavioral Inhibition, Self-Regulation of Motivation, and Working Memory in Children With Attention Deficit Hyperactivity Disorder , 2002, Developmental neuropsychology.

[59]  C. Filley The Neuroanatomy of Attention , 2002, Seminars in speech and language.

[60]  R. Tannock,et al.  Neuropsychological profiles of adolescents with ADHD: effects of reading difficulties and gender. , 2002, Journal of child psychology and psychiatry, and allied disciplines.

[61]  Marko Wilke,et al.  Correlation of white matter diffusivity and anisotropy with age during childhood and adolescence: a cross-sectional diffusion-tensor MR imaging study. , 2002, Radiology.

[62]  M. Hoptman,et al.  Frontal white matter microstructure, aggression, and impulsivity in men with schizophrenia: a preliminary study , 2002, Biological Psychiatry.

[63]  Godfrey D Pearlson,et al.  MRI parcellation of the frontal lobe in boys with attention deficit hyperactivity disorder or Tourette syndrome , 2002, Psychiatry Research: Neuroimaging.

[64]  Pratik Mukherjee,et al.  Diffusion-tensor MR imaging of normal brain maturation: a guide to structural development and myelination. , 2003, AJR. American journal of roentgenology.

[65]  Y. Miyashita,et al.  Transient Activation of Superior Prefrontal Cortex during Inhibition of Cognitive Set , 2003, The Journal of Neuroscience.

[66]  Shelley Channon,et al.  Executive function, memory, and learning in Tourette's syndrome. , 2003, Neuropsychology.

[67]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[68]  Suzanne E. Welcome,et al.  Longitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children , 2022 .

[69]  Peter Redgrave,et al.  Basal Ganglia , 2020, Encyclopedia of Autism Spectrum Disorders.