Regional White Matter Scaling in the Human Brain
- 9 July 2021
- journal article
- research article
- Published by Society for Neuroscience in Journal of Neuroscience
- Vol. 41 (33), 7015-7028
- https://doi.org/10.1523/jneurosci.1193-21.2021
Abstract
Anatomical organization of the primate cortex varies as a function of total brain size, where possession of a larger brain is accompanied by disproportionate expansion of associative cortices alongside a relative contraction of sensorimotor systems. However, equivalent scaling maps are not yet available for regional white matter anatomy. Here, we use three large-scale neuroimaging datasets to examine how regional white matter volume (WMV) scales with interindividual variation in brain volume amongst typically developing humans (combined N = 2391; 1247 females, 1144 males). We show that WMV scaling is regionally heterogeneous: larger brains have relatively greater WMV in anterior and posterior regions of cortical white matter, as well as the genu and splenium of the corpus callosum, but relatively less WMV in most subcortical regions. Furthermore, regions of positive WMV scaling tend to connect previously-defined regions of positive gray matter scaling in the cortex – revealing a coordinated coupling of regional gray and white matter organization with naturally occurring variations in human brain size. However, we also show that two commonly studied measures of white matter microstructure–fractional anisotropy (FA) and magnetization transfer (MT)–scale negatively with brain size, and do so in a manner that is spatially unlike WMV scaling. Collectively, these findings provide a more complete view of anatomical scaling in the human brain, and offer new contexts for the interpretation of regional white matter variation in health and disease. SIGNIFICANCE STATEMENT: Recent work has shown that, in humans, regional cortical and subcortical anatomy show systematic changes as a function of brain size variation. Here, we show that regional white matter structures also show brain-size related changes in humans. Specifically, white matter regions connecting higher-order cortical systems are relatively expanded in larger human brains, while subcortical and cerebellar white matter tracts responsible for unimodal sensory or motor functions are relatively contracted. This regional scaling of white matter volume is coordinated with regional scaling of cortical anatomy, but distinct from scaling of white matter microstructure. These findings provide a more complete view of anatomical scaling of the human brain, with relevance for evolutionary, basic, and clinical neuroscience.This publication has 67 references indexed in Scilit:
- Different scaling of white matter volume, cortical connectivity, and gyrification across rodent and primate brainsFrontiers in Neuroanatomy, 2013
- Quantitative multi-parameter mapping of R1, PD*, MT, and R2* at 3T: a multi-center validationFrontiers in Neuroscience, 2013
- Connectivity-driven white matter scaling and folding in primate cerebral cortexProceedings of the National Academy of Sciences of the United States of America, 2010
- Similar patterns of cortical expansion during human development and evolutionProceedings of the National Academy of Sciences of the United States of America, 2010
- Frontal White Matter Volume Is Associated with Brain Enlargement and Higher Structural Connectivity in Anthropoid PrimatesPLOS ONE, 2010
- Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registrationNeuroImage, 2009
- Functional Trade-Offs in White Matter Axonal ScalingJournal of Neuroscience, 2008
- Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM templateNeuroImage, 2008
- Evolving Knowledge of Sex Differences in Brain Structure, Function, and ChemistryBiological Psychiatry, 2007
- Sexual dimorphism of brain developmental trajectories during childhood and adolescenceNeuroImage, 2007