Selective effects of aging on brain white matter microstructure: A diffusion tensor imaging tractography study

We examined age-related changes in the cerebral white matter. Structural magnetic resonance images (MRIs) and diffusion tensor images (DTIs) were acquired from 69 healthy subjects aged 22-84 years. Quantitative DTI tractography was performed for nine different white matter tracts to determine tract volume, fractional anisotropy (FA), mean diffusivity (MD), axial, and radial diffusivities. We used automated and manual segmentation to determine volumes of gray matter (GM), white mater (WM), cerebrospinal fluid (CSF), and intracranial space. The results showed significant effects of aging on WM, GM, CSF volumes, and selective effects of aging on structural integrity of different white matter tracts. WM of the prefrontal region was the most vulnerable to aging, while temporal lobe connections, cingulum, and parieto-occipital commissural connections showed relative preservation with age. This study was cross-sectional, and therefore, additional longitudinal studies are needed to confirm our findings.

[1]  Oliver Ganslandt,et al.  Quantitative diffusion tensor fiber tracking of age-related changes in the limbic system , 2007, European Radiology.

[2]  J. Babb,et al.  Age-related total gray matter and white matter changes in normal adult brain. Part I: volumetric MR imaging analysis. , 2002, AJNR. American journal of neuroradiology.

[3]  Randy L. Gollub,et al.  Reproducibility of quantitative tractography methods applied to cerebral white matter , 2007, NeuroImage.

[4]  Paul J. Harrison,et al.  Asymmetry of the uncinate fasciculus: a post-mortem study of normal subjects and patients with schizophrenia. , 2002, Cerebral cortex.

[5]  Faith M. Gunning-Dixon,et al.  Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume , 2004, Neurobiology of Aging.

[6]  K. Lim,et al.  Age‐related decline in brain white matter anisotropy measured with spatially corrected echo‐planar diffusion tensor imaging , 2000, Magnetic resonance in medicine.

[7]  Luis Concha,et al.  Diffusion tensor imaging tractography and reliability analysis for limbic and paralimbic white matter tracts , 2008, Psychiatry Research: Neuroimaging.

[8]  C. Fennema-Notestine,et al.  Effects of age on tissues and regions of the cerebrum and cerebellum , 2001, Neurobiology of Aging.

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

[10]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

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

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

[13]  N. Raz,et al.  Differential Aging of the Brain: Patterns, Cognitive Correlates and Modifiers , 2022 .

[14]  John S. Allen,et al.  Normal neuroanatomical variation due to age: The major lobes and a parcellation of the temporal region , 2005, Neurobiology of Aging.

[16]  Bruce Fischl,et al.  Regional white matter volume differences in nondemented aging and Alzheimer's disease , 2009, NeuroImage.

[17]  Richard Camicioli,et al.  Aging hippocampus and amygdala , 2008, Neuroreport.

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

[19]  A. Dale,et al.  Age-related alterations in white matter microstructure measured by diffusion tensor imaging , 2005, Neurobiology of Aging.

[20]  Tanguy Marqueste,et al.  Echo planar diffusion tensor imaging of the mouse spinal cord at thoracic and lumbar levels: A feasibility study , 2010, Magnetic resonance in medicine.

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

[22]  S. Mori,et al.  Principles of Diffusion Tensor Imaging and Its Applications to Basic Neuroscience Research , 2006, Neuron.

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

[24]  Oliver Ganslandt,et al.  Age-related degradation in the central nervous system: assessment with diffusion-tensor imaging and quantitative fiber tracking. , 2008, Radiology.

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

[26]  Maria Assunta Rocca,et al.  Voxel-based analysis derived from fractional anisotropy images of white matter volume changes with aging , 2008, NeuroImage.

[27]  Edith V. Sullivan,et al.  Equivalent disruption of regional white matter microstructure in ageing healthy men and women , 2001, Neuroreport.

[28]  Larry A. Kramer,et al.  Diffusion tensor tractography quantification of the human corpus callosum fiber pathways across the lifespan , 2009, Brain Research.

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

[30]  J A Yesavage,et al.  Geriatric Depression Scale. , 1988, Psychopharmacology bulletin.

[31]  R. Kikinis,et al.  White matter changes with normal aging , 1998, Neurology.

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

[33]  Ronald A. Cohen,et al.  Diffusion tensor imaging of the corpus callosum: a cross-sectional study across the lifespan , 2007, International Journal of Developmental Neuroscience.

[34]  F. Schmitt,et al.  Age and gender effects on human brain anatomy: A voxel-based morphometric study in healthy elderly , 2007, Neurobiology of Aging.

[35]  E. Gordon,et al.  Cognitive aging, executive function, and fractional anisotropy: a diffusion tensor MR imaging study. , 2007, AJNR. American journal of neuroradiology.

[36]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[37]  Hangyi Jiang,et al.  DtiStudio: Resource program for diffusion tensor computation and fiber bundle tracking , 2006, Comput. Methods Programs Biomed..

[38]  Jens Frahm,et al.  Topography of the human corpus callosum revisited—Comprehensive fiber tractography using diffusion tensor magnetic resonance imaging , 2006, NeuroImage.

[39]  A. Pfefferbaum,et al.  Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber tracking. , 2006, Cerebral cortex.

[40]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

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

[42]  I. Lucki,et al.  Adult hippocampal neurogenesis: Regulation, functional implications, and contribution to disease pathology , 2009, Neuroscience & Biobehavioral Reviews.

[43]  I Litvan,et al.  The FAB: A frontal assessment battery at bedside , 2000, Neurology.

[44]  G. Bartzokis,et al.  Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study. , 2001, Archives of general psychiatry.

[45]  A. Dale,et al.  Effects of age on volumes of cortex, white matter and subcortical structures , 2005, Neurobiology of Aging.

[46]  A. Pfefferbaum,et al.  Increased brain white matter diffusivity in normal adult aging: Relationship to anisotropy and partial voluming , 2003, Magnetic resonance in medicine.

[47]  Alan Peters,et al.  The Effects of Normal Aging on Myelinated Nerve Fibers in Monkey Central Nervous System , 2009, Front. Neuroanat..

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

[49]  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.

[50]  Leanne M Williams,et al.  Preservation of limbic and paralimbic structures in aging , 2005, Human brain mapping.

[51]  Denis Le Bihan,et al.  Looking into the functional architecture of the brain with diffusion MRI , 2003, Nature Reviews Neuroscience.

[52]  Peter Seres,et al.  Three-dimensional volumetric analysis and reconstruction of amygdala and hippocampal head, body and tail , 2007, Psychiatry Research: Neuroimaging.

[53]  J. Townsend,et al.  Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. , 2000, Radiology.

[54]  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.

[55]  Haruyasu Yamada,et al.  Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis , 2002, Neurobiology of Aging.

[56]  W. Meier-Ruge,et al.  Age‐Related White Matter Atrophy in the Human Brain , 1992, Annals of the New York Academy of Sciences.

[57]  A. Dale,et al.  Age‐Related Changes in Prefrontal White Matter Measured by Diffusion Tensor Imaging , 2005, Annals of the New York Academy of Sciences.

[58]  J. Gorell,et al.  Validity of the Dementia Rating Scale in Assessing Cognitive Function in Parkinson's Disease , 1999, Journal of geriatric psychiatry and neurology.