Superficial White Matter: Effects of Age, Sex, and Hemisphere

Structural and diffusion imaging studies demonstrate effects of age, sex, and asymmetry in many brain structures. However, few studies have addressed how individual differences might influence the structural integrity of the superficial white matter (SWM), comprised of short-range association (U-fibers), and intracortical axons. This study thus applied a sophisticated computational analysis approach to structural and diffusion imaging data obtained from healthy individuals selected from the International Consortium for Brain Mapping (ICBM) database across a wide adult age range (n=65, age: 18-74 years, all Caucasian). Fractional anisotropy (FA), radial diffusivity (RD), and axial diffusivity (AD) were sampled and compared at thousands of spatially matched SWM locations and within regions-of-interest to examine global and local variations in SWM integrity across age, sex, and hemisphere. Results showed age-related reductions in FA that were more pronounced in the frontal SWM than in the posterior and ventral brain regions, whereas increases in RD and AD were observed across large areas of the SWM. FA was significantly greater in left temporoparietal regions in men and in the posterior callosum in women. Prominent leftward FA and rightward AD and RD asymmetries were observed in the temporal, parietal, and frontal regions. Results extend previous findings restricted to the deep white matter pathways to demonstrate regional changes in the SWM microstructure relating to processes of demyelination and/or to the number, coherence, or integrity of axons with increasing age. SWM fiber organization/coherence appears greater in the left hemisphere regions spanning language and other networks, while more localized sex effects could possibly reflect sex-specific advantages in information strategies.

[1]  Xiaojian Kang,et al.  Diffusion properties of cortical and pericortical tissue: regional variations, reliability and methodological issues. , 2012, Magnetic resonance imaging.

[2]  B. Pakkenberg,et al.  Marked loss of myelinated nerve fibers in the human brain with age , 2003, The Journal of comparative neurology.

[3]  Jorge Sepulcre,et al.  Evidence from intrinsic activity that asymmetry of the human brain is controlled by multiple factors , 2009, Proceedings of the National Academy of Sciences.

[4]  Arthur W. Toga,et al.  Mapping Corticocortical Structural Integrity in Schizophrenia and Effects of Genetic Liability , 2011, Biological Psychiatry.

[5]  B. Pakkenberg,et al.  Age-Induced White Matter Changes in the Human Brain: A Stereological Investigation , 1997, Neurobiology of Aging.

[6]  Joanna Jacobus,et al.  Sex differences in adolescent white matter architecture , 2011, Brain Research.

[7]  Paul M. Thompson,et al.  Fractional anisotropy of cerebral white matter and thickness of cortical gray matter across the lifespan , 2011, NeuroImage.

[8]  N. Geschwind.  The organization of language and the brain. , 1970, Science.

[9]  Usha Sinha,et al.  Exploratory voxel-based analysis of diffusion indices and hemispheric asymmetry in normal aging. , 2007, Magnetic resonance imaging.

[10]  Sterling C. Johnson,et al.  White Matter in Aging and Cognition: A Cross-Sectional Study of Microstructure in Adults Aged Eighteen to Eighty-Three , 2010, Developmental neuropsychology.

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

[12]  Alan C. Evans,et al.  Brain Connectivity , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[13]  Sukhwinder S. Shergill,et al.  Gender Differences in White Matter Microstructure , 2012, PloS one.

[14]  Andrew L. Alexander,et al.  Age- and gender-related changes in the normal human brain using hybrid diffusion imaging (HYDI) , 2011, NeuroImage.

[15]  Jung-Lung Hsu,et al.  Gender differences and age-related white matter changes of the human brain: A diffusion tensor imaging study , 2008, NeuroImage.

[16]  G. Bruce Pike,et al.  Standing-wave and RF penetration artifacts caused by elliptic geometry: an electrodynamic analysis of MRI , 1998, IEEE Transactions on Medical Imaging.

[17]  Denise C. Park,et al.  Handbook of the Psychology of Aging , 1979 .

[18]  Roberto Cabeza,et al.  Assessing the effects of age on long white matter tracts using diffusion tensor tractography , 2009, NeuroImage.

[19]  Derek K. Jones,et al.  Symmetries in human brain language pathways correlate with verbal recall , 2007, Proceedings of the National Academy of Sciences.

[20]  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.

[21]  Arthur W. Toga,et al.  Human brain white matter atlas: Identification and assignment of common anatomical structures in superficial white matter , 2008, NeuroImage.

[22]  A. Pfefferbaum,et al.  Diffusion tensor imaging and aging , 2006, Neuroscience & Biobehavioral Reviews.

[23]  Peter Seres,et al.  Selective effects of aging on brain white matter microstructure: A diffusion tensor imaging tractography study , 2010, NeuroImage.

[24]  A. Wright,et al.  Magnetic resonance microimaging of intraaxonal water diffusion in live excised lamprey spinal cord , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. H. Howard,et al.  Age‐related differences in multiple measures of white matter integrity: A diffusion tensor imaging study of healthy aging , 2009, Human brain mapping.

[26]  Arthur W. Toga,et al.  Construction of a 3D probabilistic atlas of human cortical structures , 2008, NeuroImage.

[27]  M. Ashtari,et al.  Development and aging of the healthy human brain uncinate fasciculus across the lifespan using diffusion tensor tractography , 2009, Brain Research.

[28]  N. Geschwind,et al.  Right-left asymmetrics in the brain. , 1978, Science.

[29]  B. Anderson,et al.  Anatomic asymmetries of the posterior superior temporal lobes: a postmortem study. , 1999, Neuropsychiatry, neuropsychology, and behavioral neurology.

[30]  Pierre Legendre,et al.  An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model , 1999 .

[31]  Diane C. Chugani,et al.  Diffusion Tensor Imaging of Frontal Lobe in Autism Spectrum Disorder , 2008, Cerebral cortex.

[32]  Arthur W. Toga,et al.  The myth of the normal, average human brain—The ICBM experience: (1) Subject screening and eligibility , 2009, NeuroImage.

[33]  A. Pfefferbaum,et al.  Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: Relations to timed performance , 2010, Neurobiology of Aging.

[34]  Marti J. Anderson,et al.  Permutation tests for multi-factorial analysis of variance , 2003 .

[35]  Jack L. Lancaster,et al.  Loss of cerebral white matter structural integrity tracks the gray matter metabolic decline in normal aging , 2009, NeuroImage.

[36]  V. Menon,et al.  White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. , 2005, Cerebral cortex.

[37]  Javier DeFelipe,et al.  Cortical White Matter: Beyond the Pale Remarks, Main Conclusions and Discussion , 2010, Front. Neuroanat..

[38]  Eileen Luders,et al.  Structural and functional reorganization of the corpus callosum between the age of 6 and 8 years. , 2011, Cerebral cortex.

[39]  Scott T. Grafton,et al.  Automated image registration: I. General methods and intrasubject, intramodality validation. , 1998, Journal of computer assisted tomography.

[40]  N. Intrator,et al.  Free water elimination and mapping from diffusion MRI , 2009, Magnetic resonance in medicine.

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

[42]  M. Peters,et al.  The Parallel Brain: The Cognitive Neuroscience of the Corpus Callosum , 2004 .

[43]  Xiaoping P. Hu,et al.  Asymmetric connectivity reduction and its relationship to “HAROLD” in aging brain , 2009, Brain Research.

[44]  H. Uylings,et al.  Aging does not affect gray matter asymmetry. , 2010, Psychology and aging.

[45]  Suzanne E. Welcome,et al.  Mapping cortical change across the human life span , 2003, Nature Neuroscience.

[46]  Arthur W. Toga,et al.  Cortical Sulcal Atlas Construction Using a Diffeomorphic Mapping Approach , 2010, MICCAI.

[47]  Karl J. Friston,et al.  Cerebral Asymmetry and the Effects of Sex and Handedness on Brain Structure: A Voxel-Based Morphometric Analysis of 465 Normal Adult Human Brains , 2001, NeuroImage.

[48]  Arthur W. Toga,et al.  Diffeomorphic Sulcal Shape Analysis on the Cortex , 2012, IEEE Transactions on Medical Imaging.

[49]  V. Wedeen,et al.  Reduction of eddy‐current‐induced distortion in diffusion MRI using a twice‐refocused spin echo , 2003, Magnetic resonance in medicine.

[50]  Eileen Luders,et al.  Annals of the New York Academy of Sciences Exploring Age-related Brain Degeneration in Meditation Practitioners , 2022 .

[51]  Lisa H. Lu,et al.  Relationships between brain activation and brain structure in normally developing children. , 2009, Cerebral cortex.

[52]  Thomas L Chenevert,et al.  Clinical applications of diffusion tensor imaging , 2004, Journal of magnetic resonance imaging : JMRI.

[53]  A. Toga,et al.  Mapping brain asymmetry , 2003, Nature Reviews Neuroscience.

[54]  Fang Liu,et al.  Sex differences in the human corpus callosum microstructure: A combined T2 myelin-water and diffusion tensor magnetic resonance imaging study , 2010, Brain Research.

[55]  G. Meyer,et al.  Neurons in the White Matter of the Adult Human Neocortex , 2009, Front. Neuroanat..

[56]  Timothy J. Herron,et al.  Regional variation, hemispheric asymmetries and gender differences in pericortical white matter , 2011, NeuroImage.

[57]  D. Head,et al.  Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. , 2004, Cerebral cortex.

[58]  T. Krahe,et al.  The effects of hand preference and gender on finger tapping performance asymmetry by the use of an infra-red light measurement device , 2000, Neuropsychologia.

[59]  M. Belke,et al.  Men and women are different: Diffusion tensor imaging reveals sexual dimorphism in the microstructure of the thalamus, corpus callosum and cingulum , 2011, NeuroImage.

[60]  Cecilia Parazzini,et al.  Terminal zones of myelination: MR evaluation of children aged 20-40 months. , 2002, AJNR. American journal of neuroradiology.

[61]  Larry A. Kramer,et al.  Diffusion tensor imaging-based tissue segmentation: Validation and application to the developing child and adolescent brain , 2007, NeuroImage.

[62]  R. Cabeza.  Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[63]  Arthur W. Toga,et al.  Diffeomorphic sulcal shape analysis for cortical surface registration , 2010, 2010 IEEE Computer Society Conference on Computer Vision and Pattern Recognition.

[64]  N. Geschwind.  The Organization of Language and the Brain: Language disorders after brain damage help in elucidating the neural basis of verbal behavior , 1970 .

[65]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[66]  Peter Seres,et al.  Structural organization of the prefrontal white matter pathways in the adult and aging brain measured by diffusion tensor imaging , 2011, Brain Structure and Function.

[67]  P. Thompson,et al.  Gray matter deficits, mismatch negativity, and outcomes in schizophrenia. , 2011, Schizophrenia bulletin.

[68]  C. Wheeler-Kingshott,et al.  About “axial” and “radial” diffusivities , 2009, Magnetic resonance in medicine.

[69]  Matthew F Glasser,et al.  DTI tractography of the human brain's language pathways. , 2008, Cerebral cortex.

[70]  H. Yamasue,et al.  Aging effects on cerebral asymmetry: a voxel-based morphometry and diffusion tensor imaging study. , 2010, Magnetic resonance imaging.

[71]  Arthur W. Toga,et al.  Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: Application to normal elderly and Alzheimer's disease participants , 2009, NeuroImage.

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

[73]  Michael C. Corballis,et al.  Regional differences in cerebral asymmetries of human cortical white matter , 2011, Neuropsychologia.

[74]  Luis Concha,et al.  Diffusion tensor imaging of time-dependent axonal and myelin degradation after corpus callosotomy in epilepsy patients , 2006, NeuroImage.

[75]  Derek K. Jones,et al.  How and how not to correct for CSF-contamination in diffusion MRI , 2012, NeuroImage.

[76]  J. Rapoport,et al.  Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[77]  Eileen Luders,et al.  Sex differences in brain anatomy. , 2010, Progress in brain research.

[78]  L. Westlye,et al.  Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. , 2010, Cerebral cortex.

[79]  A. Parent,et al.  Carpenter's Human Neuroanatomy , 1996 .

[80]  In Chan Song,et al.  Tractography-guided statistics (TGIS) in diffusion tensor imaging for the detection of gender difference of fiber integrity in the midsagittal and parasagittal corpora callosa , 2007, NeuroImage.

[81]  H Takao,et al.  Effects of Age and Gender on White Matter Integrity , 2011, American Journal of Neuroradiology.

[82]  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.

[83]  David H. Miller,et al.  Quantitative magnetic resonance of postmortem multiple sclerosis brain before and after fixation , 2008, Magnetic resonance in medicine.

[84]  C. Pierpaoli,et al.  Characterization of and correction for eddy current artifacts in echo planar diffusion imaging , 1998, Magnetic resonance in medicine.

[85]  Georg Winterer,et al.  Disturbed structural connectivity in schizophrenia primary factor in pathology or epiphenomenon? , 2007, Schizophrenia bulletin.

[86]  J. Mazziotta,et al.  Automated image registration , 1993 .

[87]  Tutis Vilis,et al.  Task-related laterality effects in the lateral occipital complex , 2007, Brain Research.

[88]  Michael I. Miller,et al.  Atlas-based analysis of neurodevelopment from infancy to adulthood using diffusion tensor imaging and applications for automated abnormality detection , 2010, NeuroImage.

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

[90]  A. Dale,et al.  Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. , 2010, Cerebral cortex.

[91]  N. Raz,et al.  Aging white matter and cognition: Differential effects of regional variations in diffusion properties on memory, executive functions, and speed , 2009, Neuropsychologia.

[92]  R. Leahy,et al.  Magnetic Resonance Image Tissue Classification Using a Partial Volume Model , 2001, NeuroImage.

[93]  A. Ohnishi,et al.  Apparent diffusion coefficient on rat brain and nerves intoxicated with methylmercury. , 1999, Environmental research.

[94]  Christian Beaulieu,et al.  Diffusion anisotropy in subcortical white matter and cortical gray matter: Changes with aging and the role of CSF‐suppression , 2004, Journal of magnetic resonance imaging : JMRI.

[95]  Eileen Luders,et al.  Asymmetries of cortical thickness: effects of handedness, sex, and schizophrenia , 2007, Neuroreport.

[96]  Shu-Wei Sun,et al.  The MT pool size ratio and the DTI radial diffusivity may reflect the myelination in shiverer and control mice , 2009, NMR in biomedicine.

[97]  K. Ohtomo,et al.  White matter asymmetry in healthy individuals: a diffusion tensor imaging study using tract-based spatial statistics , 2011, Neuroscience.

[98]  C. Lebel,et al.  Diffusion tensor imaging of white matter tract evolution over the lifespan , 2012, NeuroImage.

[99]  F. Craik,et al.  The handbook of aging and cognition (3rd ed.). , 2008 .

[100]  Paul M. Thompson,et al.  journal homepage: www.elsevier.com/locate/ynimg Genetic influences on brain asymmetry: A DTI study of 374 twins and siblings , 2022 .

[101]  Reto Meuli,et al.  Demyelination of superficial white matter in early Alzheimer's disease: a magnetization transfer imaging study , 2012, Neurobiology of Aging.

[102]  J C Mazziotta,et al.  Automated image registration: II. Intersubject validation of linear and nonlinear models. , 1998, Journal of computer assisted tomography.

[103]  Arthur W Toga,et al.  Topographical relationships between arcuate fasciculus connectivity and cortical thickness , 2011, Human brain mapping.

[104]  R. Kahn,et al.  Human brain changes across the life span: A review of 56 longitudinal magnetic resonance imaging studies , 2012, Human brain mapping.

[105]  Hauke R. Heekeren,et al.  Age-related differences in white matter microstructure: Region-specific patterns of diffusivity , 2010, NeuroImage.