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      Lifespan maturation and degeneration of human brain white matter

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          Abstract

          Properties of human brain tissue change across the lifespan. Here we model these changes in the living human brain by combining quantitative MRI measurements of R1 (1/T1) with diffusion MRI and tractography (N=102, ages 7–85). The amount of R1 change during development differs between white matter fascicles, but in each fascicle the rate of development and decline are mirror symmetric; the rate of R1 development as the brain approaches maturity predicts the rate of R1 degeneration in aging. Quantitative measurements of macromolecule tissue volume (MTV) confirm that R1 is an accurate index of the growth of new brain tissue. In contrast to R1, diffusion development follows an asymmetric time-course with rapid childhood changes but a slow rate of decline in old age. Together, the time-courses of R1 and diffusion changes demonstrate that multiple biological processes drive changes in white matter tissue properties over the lifespan.

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          White matter in learning, cognition and psychiatric disorders.

          R. Douglas Fields (2008)
          White matter is the brain region underlying the gray matter cortex, composed of neuronal fibers coated with electrical insulation called myelin. Previously of interest in demyelinating diseases such as multiple sclerosis, myelin is attracting new interest as an unexpected contributor to a wide range of psychiatric disorders, including depression and schizophrenia. This is stimulating research into myelin involvement in normal cognitive function, learning and IQ. Myelination continues for decades in the human brain; it is modifiable by experience, and it affects information processing by regulating the velocity and synchrony of impulse conduction between distant cortical regions. Cell-culture studies have identified molecular mechanisms regulating myelination by electrical activity, and myelin also limits the critical period for learning through inhibitory proteins that suppress axon sprouting and synaptogenesis.
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            Longitudinal development of human brain wiring continues from childhood into adulthood.

            Catherine Lebel, Christian Beaulieu (2011)
            Healthy human brain development is a complex process that continues during childhood and adolescence, as demonstrated by many cross-sectional and several longitudinal studies. However, whether these changes end in adolescence is not clear. We examined longitudinal white matter maturation using diffusion tensor tractography in 103 healthy subjects aged 5-32 years; each volunteer was scanned at least twice, with 221 total scans. Fractional anisotropy (FA) and mean diffusivity (MD), parameters indicative of factors including myelination and axon density, were assessed in 10 major white matter tracts. All tracts showed significant nonlinear development trajectories for FA and MD. Significant within-subject changes occurred in the vast majority of children and early adolescents, and these changes were mostly complete by late adolescence for projection and commissural tracts. However, association tracts demonstrated postadolescent within-subject maturation of both FA and MD. Diffusion parameter changes were due primarily to decreasing perpendicular diffusivity, although increasing parallel diffusivity contributed to the prolonged increases of FA in association tracts. Volume increased significantly with age for most tracts, and longitudinal measures also demonstrated postadolescent volume increases in several association tracts. As volume increases were not directly associated with either elevated FA or reduced MD between scans, the observed diffusion parameter changes likely reflect microstructural maturation of brain white matter tracts rather than just gross anatomy.
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              Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry.

              Lars T. Westlye, Kristine B. Walhovd, Anders Dale … (2010)
              Magnetic resonance imaging volumetry studies report inverted U-patterns with increasing white-matter (WM) volume into middle age suggesting protracted WM maturation compared with the cortical gray matter. Diffusion tensor imaging (DTI) is sensitive to degree and direction of water permeability in biological tissues, providing in vivo indices of WM microstructure. The aim of this cross-sectional study was to delineate age trajectories of WM volume and DTI indices in 430 healthy subjects ranging 8-85 years of age. We used automated regional brain volume segmentation and tract-based statistics of fractional anisotropy, mean, and radial diffusivity as markers of WM integrity. Nonparametric regressions were used to fit the age trajectories and to estimate the timing of maximum development and deterioration in aging. Although the volumetric data supported protracted growth into the sixth decade, DTI indices plateaued early in the fourth decade across all tested regions and then declined slowly into late adulthood followed by an accelerating decrease in senescence. Tractwise and voxel-based analyses yielded regional differences in development and aging but did not provide ample evidence in support of a simple last-in-first-out hypothesis of life-span changes.
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                Author and article information

                Journal
                Journal ID (nlm-journal-id): 101528555
                Journal ID (pubmed-jr-id): 37539
                Journal ID (nlm-ta): Nat Commun
                Journal ID (iso-abbrev): Nat Commun
                Title: Nature communications
                ISSN (Electronic): 2041-1723
                Publication date Nihms-submitted: 15 November 2014
                Publication date (Electronic): 17 September 2014
                Publication date Collection: 2014
                Publication date PMC-release: 17 March 2015
                Volume: 5
                Page: 4932
                Affiliations
                [1 ]Stanford University Department of Psychology, Stanford, CA, USA
                [2 ]Stanford University Center for Cognitive and Neurobiological Imaging, Stanford, CA, USA
                [3 ]Hebrew University Edmond and Lily Safra Center for Brain Sciences (ELSC), Jerusalm, Israel
                Author notes
                Corresponding Authors: Jason D. Yeatman, jdyeatman@ 123456gmail.com , Department of Psychology, Stanford University, Jordan Hall, 450 Serra Mall, Stanford, Ca, 94305. Aviv A. Mezer, Aviv.Mezer@ 123456ELSC.huji.ac.il , Edmond and Lily Safra Center for Brain Sciences (ELSC), The Hebrew University, Givat Ram, Jerusalem 91904. Israel
                Article
                Manuscript ID: NIHMS620353
                DOI: 10.1038/ncomms5932
                PMC ID: 4238904
                PubMed ID: 25230200
                SO-VID: e754ca17-1277-4e80-a083-9f759e694ccd
                History
                Categories
                Subject: Article

                ScienceOpen disciplines: Uncategorized
                Keywords: quantitative magnetic resonance imaging (qmri),r1,t1,diffusion weighted imaging (dwi),mean diffusivity,white matter,fascicle,myelin,development,aging,multiple sclerosis (ms)
                Data availability:
                ScienceOpen disciplines: Uncategorized
                Keywords: quantitative magnetic resonance imaging (qmri), r1, t1, diffusion weighted imaging (dwi), mean diffusivity, white matter, fascicle, myelin, development, aging, multiple sclerosis (ms)

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