Age-related regional variations of the corpus callosum identified by diffusion tensor tractography

The corpus callosum is the largest white matter connection in the human brain, and an understanding of its evolution with age in healthy individuals is one crucial aspect for determining its role in cognition and disease. Diffusion tensor imaging (DTI) allows for investigation of age-related callosal changes since tractography can both virtually reconstruct the segments of the corpus callosum in vivo based on unique target cortical regions, and provide quantitative diffusion parameters reflecting tissue microstructure. DTI tractography was used to subdivide the corpus callosum into seven distinct sections based on unique target areas (i.e., orbital frontal, anterior frontal, superior frontal, superior parietal, posterior parietal, temporal, and occipital) in a very large number of healthy volunteers (n=315) across a wide age range (5-59 years). Both fractional anisotropy (FA) and mean diffusivity (MD) changes with respect to age were fit with Poisson curves, showing increasing FA and decreasing MD during childhood and adolescence and slightly slower decreases of FA and increases of MD at older ages. Age at peak FA values and minimum MD values varied from 21 to 44 years, and an overall "outer-to-inner" trend was observed in which the anterior and posterior regions peaked earlier than central areas. In addition to these maturational trends of diffusion parameters reflecting the microstructural changes in the healthy corpus callosum over a large age range spanning childhood to older adulthood, these results can provide a baseline for identifying the presence and timing of callosal abnormalities in various brain disorders.

[1]  R. Gorski,et al.  Sex differences in the corpus callosum of the living human being , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[4]  F. Groenendaal,et al.  Corpus Callosum Size in Relation to Motor Performance in 9- to 10-Year-Old Children with Neonatal Encephalopathy , 2008, Pediatric Research.

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

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

[7]  Jun Yoshino,et al.  Demyelination increases radial diffusivity in corpus callosum of mouse brain , 2005, NeuroImage.

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

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

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

[11]  J. Jeret,et al.  Clinicopathological Findings Associated with Agenesis of the Corpus Callosum , 1987, Brain and Development.

[12]  Jagath C. Rajapakse,et al.  Regional MRI measurements of the corpus callosum: a methodological and developmental study , 1996, Brain and Development.

[13]  Takayuki Obata,et al.  Age-related degeneration of corpus callosum measured with diffusion tensor imaging , 2006, NeuroImage.

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

[15]  Timothy Edward John Behrens,et al.  Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills , 2007, NeuroImage.

[16]  Jung-Lung Hsu,et al.  Microstructural white matter changes in normal aging: A diffusion tensor imaging study with higher-order polynomial regression models , 2010, NeuroImage.

[17]  Laura M. Stapleton,et al.  Reading and the corpus callosum: an MRI family study of volume and area. , 2007, Neuropsychology.

[18]  Marie T. Banich,et al.  Relationship between intelligence and the size and composition of the corpus callosum , 2008, Experimental Brain Research.

[19]  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.

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

[21]  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.

[22]  Jerry L. Prince,et al.  Effects of diffusion weighting schemes on the reproducibility of DTI-derived fractional anisotropy, mean diffusivity, and principal eigenvector measurements at 1.5T , 2007, NeuroImage.

[23]  Visualization of maturation of the corpus callosum during childhood and adolescence using T2 relaxometry , 2007, International Journal of Developmental Neuroscience.

[24]  Scott T. Grafton,et al.  Structural Organization of the Corpus Callosum Predicts the Extent and Impact of Cortical Activity in the Nondominant Hemisphere , 2008, The Journal of Neuroscience.

[25]  Khader M Hasan,et al.  Diffusion tensor quantification of the macrostructure and microstructure of human midsagittal corpus callosum across the lifespan , 2008, NMR in biomedicine.

[26]  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.

[27]  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.

[28]  Scott A. Huettel,et al.  Age-related slowing of memory retrieval: Contributions of perceptual speed and cerebral white matter integrity , 2008, Neurobiology of Aging.

[29]  M. Moseley Diffusion tensor imaging and aging – a review , 2002, NMR in biomedicine.

[30]  Talma Hendler,et al.  Normal white matter development from infancy to adulthood: Comparing diffusion tensor and high b value diffusion weighted MR images , 2005, Journal of magnetic resonance imaging : JMRI.

[31]  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.

[32]  Vincent J Schmithorst,et al.  Developmental differences in white matter architecture between boys and girls , 2008, Human brain mapping.

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

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

[35]  René Westerhausen,et al.  The influence of handedness and gender on the microstructure of the human corpus callosum: a diffusion-tensor magnetic resonance imaging study , 2003, Neuroscience Letters.

[36]  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.

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

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

[39]  P. Sachdev,et al.  Diffusion tensor imaging in mild cognitive impairment and Alzheimer's disease: a review , 2008, Current opinion in neurology.

[40]  F. Barkhof,et al.  Histopathologic correlates of white matter changes on MRI in Alzheimer's disease and normal aging , 1995, Neurology.

[41]  Chun-Hung Yeh,et al.  Probabilistic topography of human corpus callosum using cytoarchitectural parcellation and high angular resolution diffusion imaging tractography , 2009, Human brain mapping.

[42]  Larry A. Kramer,et al.  Diffusion tensor quantification of the human midsagittal corpus callosum subdivisions across the lifespan , 2008, Brain Research.

[43]  Derek K. Jones,et al.  Diffusion tensor MRI of the corpus callosum and cognitive function in adults born preterm , 2009, Neuroreport.

[44]  F. Aboitiz,et al.  Age-related changes in fibre composition of the human corpus callosum: sex differences. , 1996, Neuroreport.

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

[46]  Derek K. Jones,et al.  The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: A Monte Carlo study † , 2004, Magnetic resonance in medicine.

[47]  Alan C. Evans,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2000, Nature.

[48]  S. F. Witelson Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. , 1989, Brain : a journal of neurology.

[49]  Wang Zhan,et al.  Patterns of age-related water diffusion changes in human brain by concordance and discordance analysis , 2010, Neurobiology of Aging.

[50]  Brian A Wandell,et al.  Temporal-callosal pathway diffusivity predicts phonological skills in children , 2007, Proceedings of the National Academy of Sciences.

[51]  Hao Huang,et al.  DTI tractography based parcellation of white matter: Application to the mid-sagittal morphology of corpus callosum , 2005, NeuroImage.

[52]  A. Scheibel,et al.  Fiber composition of the human corpus callosum , 1992, Brain Research.

[53]  Heidi Johansen-Berg,et al.  Functional anatomy of interhemispheric cortical connections in the human brain , 2006, Journal of anatomy.

[54]  D E Grobbee,et al.  Larger corpus callosum size with better motor performance in prematurely born children. , 2004, Seminars in perinatology.

[55]  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.

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