Developmental increases in white matter network controllability support a growing diversity of brain dynamics

Evelyn Tang,Ari E Kahn,Kosha Ruparel,Danielle S Bassett,Theodore D Satterthwaite,Graham L Baum,Raquel E Gur,Tyler M Moore,Chad Giusti,Ruben C Gur,Eli Pollock,Shi Gu,David R Roalf

doi:10.1038/s41467-017-01254-4

Evelyn Tang, Ari E Kahn + Show 11 more

Open Access

https://doi.org/10.1038/s41467-017-01254-4

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Journal: Nature Communications	Publication Date: Nov 1, 2017
Citations: 216	License type: open-access

Affiliation: University of Pennsylvania

Abstract

As the human brain develops, it increasingly supports coordinated control of neural activity. The mechanism by which white matter evolves to support this coordination is not well understood. Here we use a network representation of diffusion imaging data from 882 youth ages 8–22 to show that white matter connectivity becomes increasingly optimized for a diverse range of predicted dynamics in development. Notably, stable controllers in subcortical areas are negatively related to cognitive performance. Investigating structural mechanisms supporting these changes, we simulate network evolution with a set of growth rules. We find that all brain networks are structured in a manner highly optimized for network control, with distinct control mechanisms predicted in child vs. older youth. We demonstrate that our results cannot be explained by changes in network modularity. This work reveals a possible mechanism of human brain development that preferentially optimizes dynamic network control over static network architecture.

Highlights

As the human brain develops, it increasingly supports coordinated control of neural activity
We examine controllability and synchronizability in structural brain networks derived from diffusion tensor imaging data, which we have represented as weighted adjacency matrices or graphs
We address the fundamental question of how the architecture of the brain supports the emergence of cognitive abilities in humans

Summary

Introduction

As the human brain develops, it increasingly supports coordinated control of neural activity. White matter tracts form a large-scale wiring diagram or connectome thought to support the brain’s diverse dynamics[1,2] This architecture changes as children mature into adults[3], potentially facilitating the emergence of adult cognitive function[4]. Despite the intuitive relationship between network structure and brain function[5], a fundamental mechanistic theory explaining the development of white matter organization and its relationship to emerging cognition in humans have remained elusive. We define a given subject’s capacity to alter its topology towards increasingly diverse dynamics by extracting parameters that govern the speed, extent and fall-off of network optimization These novel statistics allow us to assess whether children’s brains have greater potential for increasing their ability to move from one mental state to another (controllability).

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