Abstract

The human brain develops with a nonlinear contraction of gray matter across late childhood and adolescence with a concomitant increase in white matter volume. Across the adult population, properties of cortical gray matter covary within networks that may represent organizational units for development and degeneration. Although gray matter covariance may be strongest within structurally connected networks, the relationship to volume changes in white matter remains poorly characterized. In the present study we examined age-related trends in white and gray matter volume using T1-weighted MR images from 360 human participants from the NIH MRI study of Normal Brain Development. Images were processed through a voxel-based morphometry pipeline. Linear effects of age on white and gray matter volume were modeled within four age bins, spanning 4-18 years, each including 90 participants (45 male). White and gray matter age-slope maps were separately entered into k-means clustering to identify regions with similar age-related variability across the four age bins. Four white matter clusters were identified, each with a dominant direction of underlying fibers: anterior–posterior, left–right, and two clusters with superior–inferior directions. Corresponding, spatially proximal, gray matter clusters encompassed largely cerebellar, fronto-insular, posterior, and sensorimotor regions, respectively. Pairs of gray and white matter clusters followed parallel slope trajectories, with white matter changes generally positive from 8 years onward (indicating volume increases) and gray matter negative (decreases). As developmental disorders likely target networks rather than individual regions, characterizing typical coordination of white and gray matter development can provide a normative benchmark for understanding atypical development.

Highlights

  • As the brain develops across late childhood and adolescence, a pattern of white matter expansion (Giedd et al, 1999; Paus et al, 1999; Sowell et al, 2002; Taki et al, 2013) and gray matter contraction (Sowell et al, 2003, 2004; Gogtay et al, 2004; Shaw et al, 2008) has been observed

  • White matter clustersa showed a peak silhouette value at the four-cluster solution and gray matter clustersb at the two-cluster solution

  • The four identified white matter clusters each showed a dominant orientation of fibers, and could be uniquely matched to a spatially proximal gray matter volume cluster

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Summary

Introduction

As the brain develops across late childhood and adolescence, a pattern of white matter expansion (Giedd et al, 1999; Paus et al, 1999; Sowell et al, 2002; Taki et al, 2013) and gray matter contraction (Sowell et al, 2003, 2004; Gogtay et al, 2004; Shaw et al, 2008) has been observed. Distributed cortical regions show correlated anatomical features across the population (Mechelli et al, 2005; Lerch et al, 2006; Chen et al, 2008; Tijms et al, 2012; Alexander-Bloch et al, 2013b; Evans, 2013) in networks similar to those defined by resting state functional connectivity (Segall et al, 2012; Alexander-Bloch et al, 2013b) and white matter tractography (Gong et al, 2012) These findings have been extended to describe coordinated cortical development across childhood and adolescence (Zielinski et al, 2010; Raznahan et al, 2011b; Alexander-Bloch et al, 2013b, 2014; Khundrakpam et al, 2013). The importance of these findings is underscored by the suggestion that neurodegenerative, psychiatric, and Received January 11, 2015; accepted April 30, 2015; First published July 01, 2015. 1C.L.’s spouse is an employee of General Electric Healthcare. 2Author Contributions: S.B. designed research, analyzed data and wrote the paper; M.K. and C.C. analyzed data and wrote the paper; C.L. analyzed data and wrote the paper

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