Quantitative tract-based white matter development from birth to age 2years

Few large-scale studies have been done to characterize the normal human brain white matter growth in the first years of life. We investigated white matter maturation patterns in major fiber pathways in a large cohort of healthy young children from birth to age two using diffusion parameters fractional anisotropy (FA), radial diffusivity (RD) and axial diffusivity (RD). Ten fiber pathways, including commissural, association and projection tracts, were examined with tract-based analysis, providing more detailed and continuous spatial developmental patterns compared to conventional ROI based methods. All DTI data sets were transformed to a population specific atlas with a group-wise longitudinal large deformation diffeomorphic registration approach. Diffusion measurements were analyzed along the major fiber tracts obtained in the atlas space. All fiber bundles show increasing FA values and decreasing radial and axial diffusivities during development in the first 2years of life. The changing rates of the diffusion indices are faster in the first year than the second year for all tracts. RD and FA show larger percentage changes in the first and second years than AD. The gender effects on the diffusion measures are small. Along different spatial locations of fiber tracts, maturation does not always follow the same speed. Temporal and spatial diffusion changes near cortical regions are in general smaller than changes in central regions. Overall developmental patterns revealed in our study confirm the general rules of white matter maturation. This work shows a promising framework to study and analyze white matter maturation in a tract-based fashion. Compared to most previous studies that are ROI-based, our approach has the potential to discover localized development patterns associated with fiber tracts of interest.

[1]  Mark H. Johnson,et al.  Mapping Infant Brain Myelination with Magnetic Resonance Imaging , 2011, The Journal of Neuroscience.

[2]  Larry A Kramer,et al.  Predicting Behavioral Deficits in Pediatric Traumatic Brain Injury Through Uncinate Fasciculus Integrity , 2011, Journal of the International Neuropsychological Society.

[3]  Lucie Hertz-Pannier,et al.  Assessment of the early organization and maturation of infants' cerebral white matter fiber bundles: A feasibility study using quantitative diffusion tensor imaging and tractography , 2006, NeuroImage.

[4]  Boreom Lee,et al.  White matter neuroplastic changes in long-term trained players of the game of “Baduk” (GO): A voxel-based diffusion-tensor imaging study , 2010, NeuroImage.

[5]  Roland G. Henry,et al.  Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns , 2004, NeuroImage.

[6]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[7]  R. Kikinis,et al.  Fronto–Temporal Disconnectivity in Schizotypal Personality Disorder: A Diffusion Tensor Imaging Study , 2005, Biological Psychiatry.

[8]  J. K. Smith,et al.  Early Postnatal Development of Corpus Callosum and Corticospinal White Matter Assessed with Quantitative Tractography , 2007, American Journal of Neuroradiology.

[9]  Rebecca C. Knickmeyer,et al.  A Structural MRI Study of Human Brain Development from Birth to 2 Years , 2008, The Journal of Neuroscience.

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

[11]  Gregor Kasprian,et al.  In utero tractography of fetal white matter development , 2008, NeuroImage.

[12]  M. Raichle,et al.  Tracking neuronal fiber pathways in the living human brain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[14]  Guido Gerig,et al.  Unbiased diffeomorphic atlas construction for computational anatomy , 2004, NeuroImage.

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

[16]  H. Kinney,et al.  Sequence of Central Nervous System Myelination in Human Infancy. II. Patterns of Myelination in Autopsied Infants , 1988, Journal of neuropathology and experimental neurology.

[17]  Bradley S Peterson,et al.  Brain Imaging Studies of the Anatomical and Functional Consequences of Preterm Birth for Human Brain Development , 2003, Annals of the New York Academy of Sciences.

[18]  Guido Gerig,et al.  Fiber tract-oriented statistics for quantitative diffusion tensor MRI analysis. , 2006, Medical image computing and computer-assisted intervention : MICCAI ... International Conference on Medical Image Computing and Computer-Assisted Intervention.

[19]  John H. Gilmore,et al.  Group analysis of DTI fiber tract statistics with application to neurodevelopment , 2009, NeuroImage.

[20]  Nobusada Shinoura,et al.  Right temporal lobe plays a role in verbal memory , 2011, Neurological research.

[21]  G. Gamkrelidze,et al.  Developmental Changes in Diffusion Anisotropy Coincide with Immature Oligodendrocyte Progression and Maturation of Compound Action Potential , 2005, The Journal of Neuroscience.

[22]  Christian Beaulieu,et al.  Diffusion tensor imaging of neurodevelopment in children and young adults , 2005, NeuroImage.

[23]  J Fiehler,et al.  Evidence of Rapid Ongoing Brain Development Beyond 2 Years of Age Detected by Fiber Tracking , 2008, American Journal of Neuroradiology.

[24]  Timothy E. J. Behrens,et al.  The evolution of the arcuate fasciculus revealed with comparative DTI , 2008, Nature Neuroscience.

[25]  Yi Wang,et al.  Quality control of diffusion weighted images , 2010, Medical Imaging.

[26]  Guido Gerig,et al.  Particle Based Shape Regression of Open Surfaces with Applications to Developmental Neuroimaging , 2009, MICCAI.

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

[28]  J K Smith,et al.  Temporal and Spatial Development of Axonal Maturation and Myelination of White Matter in the Developing Brain , 2008, American Journal of Neuroradiology.

[29]  Dinggang Shen,et al.  Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects , 2009, Proceedings of the National Academy of Sciences.

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

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

[32]  D. Le Bihan,et al.  Structural Asymmetries in the Infant Language and Sensori-motor Networks , 2022 .

[33]  J. H. Gilmore,et al.  Synaptophysin and postsynaptic density protein 95 in the human prefrontal cortex from mid-gestation into early adulthood , 2007, Neuroscience.

[34]  P. Poulet,et al.  Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging , 2006, Journal of neuroscience research.

[35]  John H. Gilmore,et al.  Quantitative Analysis of White Matter Fiber Properties along Geodesic Paths , 2003, MICCAI.

[36]  T. Auton Applied Functional Data Analysis: Methods and Case Studies , 2004 .

[37]  H. Yamasue,et al.  Gray and white matter asymmetries in healthy individuals aged 21–29 years: A voxel‐based morphometry and diffusion tensor imaging study , 2011, Human brain mapping.

[38]  D DIRKS,et al.  PERCEPTION OF DICHOTIC AND MONAURAL VERBAL MATERIAL AND CEREBRAL DOMINANCE FOR SPEECH. , 1964, Acta oto-laryngologica.

[39]  B. Silverman,et al.  Nonparametric Regression and Generalized Linear Models: A roughness penalty approach , 1993 .

[40]  A. Snyder,et al.  Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. , 1998, Radiology.

[41]  R. E. Schmidt,et al.  Toward accurate diagnosis of white matter pathology using diffusion tensor imaging , 2007, Magnetic resonance in medicine.

[42]  Rebecca D Folkerth,et al.  Axonal development in the cerebral white matter of the human fetus and infant , 2005, The Journal of comparative neurology.

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

[44]  W. Kaiser,et al.  Diffusion tensor imaging: the normal evolution of ADC, RA, FA, and eigenvalues studied in multiple anatomical regions of the brain , 2009, Neuroradiology.

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

[46]  John H. Gilmore,et al.  Improved Correspondence for DTI Population Studies Via Unbiased Atlas Building , 2006, MICCAI.

[47]  Stefan Skare,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Extensive Blockinpiano Blockinpracticing Blockinhas Blockinregionally Specific Blockineffects Blockinon Blockinwhite Blockinmatter Blockindevelopment , 2022 .

[48]  Nathalie Tzourio-Mazoyer,et al.  New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. , 2005, Brain : a journal of neurology.

[49]  P. Hüppi,et al.  Diffusion tensor imaging of normal and injured developing human brain ‐ a technical review , 2002, NMR in biomedicine.

[50]  J. Bolton,et al.  Anatomie des menschlichen Gehirns und Ruckenmarks auf myelogenetischer Gründlage , 1921 .

[51]  P. F. Buckley Prenatal and Neonatal Brain Structure and White Matter Maturation in Children at High Risk for Schizophrenia , 2012 .

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

[53]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[54]  D. Geschwind,et al.  Early Asymmetry of Gene Transcription in Embryonic Human Left and Right Cerebral Cortex , 2005, Science.

[55]  Susumu Mori,et al.  Fiber tracking: principles and strategies – a technical review , 2002, NMR in biomedicine.

[56]  R. Gur,et al.  Leftward asymmetry in relative fiber density of the arcuate fasciculus , 2005, Neuroreport.

[57]  Wensheng Guo Functional Mixed Effects Models , 2002 .

[58]  D. Pandya,et al.  Cerebral White Matter — Historical Evolution of Facts and Notions Concerning the Organization of the Fiber Pathways of the Brain , 2007, Journal of the history of the neurosciences.

[59]  Manuel Lopes,et al.  Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. , 2002, Brain : a journal of neurology.

[60]  K. A. Il’yasov,et al.  Fast quantitative diffusion-tensor imaging of cerebral white matter from the neonatal period to adolescence , 2004, Neuroradiology.

[61]  L. Lagae,et al.  Construction of a stereotaxic DTI atlas with full diffusion tensor information for studying white matter maturation from childhood to adolescence using tractography‐based segmentations , 2009, Human brain mapping.

[62]  L. Younes,et al.  On the metrics and euler-lagrange equations of computational anatomy. , 2002, Annual review of biomedical engineering.

[63]  C R Bird,et al.  MR assessment of myelination in infants and children: usefulness of marker sites. , 1989, AJNR. American journal of neuroradiology.

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

[65]  B. Luna,et al.  White matter development in adolescence: a DTI study. , 2010, Cerebral cortex.

[66]  H. Duffau,et al.  Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. , 2007, Brain : a journal of neurology.

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

[68]  N. Ayache,et al.  Log‐Euclidean metrics for fast and simple calculus on diffusion tensors , 2006, Magnetic resonance in medicine.

[69]  D. Le Bihan,et al.  Diffusion tensor imaging: Concepts and applications , 2001, Journal of magnetic resonance imaging : JMRI.

[70]  J. Kucharczyk,et al.  Identification of “Premyelination” by Diffusion‐Weighted MRI , 1995, Journal of computer assisted tomography.

[71]  H. Kinney,et al.  Myelination in the developing human brain: Biochemical correlates , 1994, Neurochemical Research.

[72]  P. Thomas Fletcher,et al.  Principal geodesic analysis for the study of nonlinear statistics of shape , 2004, IEEE Transactions on Medical Imaging.

[73]  S. Maier,et al.  Microstructural Development of Human Newborn Cerebral White Matter Assessed in Vivo by Diffusion Tensor Magnetic Resonance Imaging , 1998, Pediatric Research.

[74]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

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

[76]  E. Duchesnay,et al.  Asynchrony of the early maturation of white matter bundles in healthy infants: Quantitative landmarks revealed noninvasively by diffusion tensor imaging , 2008, Human brain mapping.

[77]  Guido Gerig,et al.  Measures for validation of DTI tractography , 2012, Medical Imaging.

[78]  B. Brody,et al.  Sequence of Central Nervous System Myelination in Human Infancy. I. An Autopsy Study of Myelination , 1987, Journal of neuropathology and experimental neurology.

[79]  Susumu Mori,et al.  Diffusion Tensor Magnetic Resonance Imaging of Wallerian Degeneration in Rat Spinal Cord after Dorsal Root Axotomy , 2009, The Journal of Neuroscience.

[80]  Giorgio M. Innocenti,et al.  Exuberance in the development of cortical networks , 2005, Nature Reviews Neuroscience.

[81]  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.

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

[83]  L. Luo,et al.  Axon retraction and degeneration in development and disease. , 2005, Annual review of neuroscience.

[84]  A. Snyder,et al.  Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. , 2002, AJNR. American journal of neuroradiology.

[85]  Jin-Ting Zhang,et al.  Statistical inferences for functional data , 2007, 0708.2207.

[86]  Robert T. Leshner,et al.  Remyelination in the Human Central Nervous System , 1989, Journal of neuropathology and experimental neurology.

[87]  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.

[88]  Webb Haymaker,et al.  Histology and Histopathology of the Nervous System , 1982 .

[89]  Massimo Filippi,et al.  Language networks in semantic dementia. , 2010, Brain : a journal of neurology.

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

[91]  D. Cox Nonparametric Regression and Generalized Linear Models: A roughness penalty approach , 1993 .