Abstract

Understanding the development of human brain organization is critical for gaining insight into how the enhancement of cognitive processes is related to the fine-tuning of the brain network. However, the developmental trajectory of the large-scale white matter (WM) network is not fully understood. Here, using graph theory, we examine developmental changes in the organization of WM networks in 180 typically-developing participants. WM networks were constructed using whole brain tractography and 78 cortical regions of interest were extracted from each participant. The subjects were first divided into 5 equal sample size (n = 36) groups (early childhood: 6.0–9.7 years; late childhood: 9.8–12.7 years; adolescence: 12.9–17.5 years; young adult: 17.6–21.8 years; adult: 21.9–29.6 years). Most prominent changes in the topological properties of developing brain networks occur at late childhood and adolescence. During late childhood period, the structural brain network showed significant increase in the global efficiency but decrease in modularity, suggesting a shift of topological organization toward a more randomized configuration. However, while preserving most topological features, there was a significant increase in the local efficiency at adolescence, suggesting the dynamic process of rewiring and rebalancing brain connections at different growth stages. In addition, several pivotal hubs were identified that are vital for the global coordination of information flow over the whole brain network across all age groups. Significant increases of nodal efficiency were present in several regions such as precuneus at late childhood. Finally, a stable and functionally/anatomically related modular organization was identified throughout the development of the WM network. This study used network analysis to elucidate the topological changes in brain maturation, paving the way for developing novel methods for analyzing disrupted brain connectivity in neurodevelopmental disorders.

Highlights

  • Neuroimaging studies have demonstrated widespread and regionally specific structural and functional brain changes during development from infancy to adulthood

  • The analysis of the structural brain network constructed from regional cortical thickness correlations has revealed a non-linear developmental pattern in network metrics and that most topological changes happen at the late childhood stage (Khundrakpam et al, 2013)

  • We found that age has an incremental effect on both the fiber number (FN) and sparsity, where both increase by a factor of ∼1.6 and ∼1.2, respectively, from age 6 to 30 years

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Summary

Introduction

Neuroimaging studies have demonstrated widespread and regionally specific structural and functional brain changes during development from infancy to adulthood. Structural magnetic resonance imaging (MRI) studies have reported age-related changes in brain volumes (Giedd et al, 1999; Good et al, 2001), areas (Thompson et al, 2000), cortical thickness (Sowell et al, 2004; Shaw et al, 2008), and regional gray matter (GM) and white matter (WM) density (Paus et al, 1999; Gogtay et al, 2004). Several functional brain network studies have reported age-related increases in the small-worldness (Wu et al, 2013) and a progression from local to distributed organization (Fair et al, 2009) in brain development. The analysis of the structural brain network constructed from regional cortical thickness correlations has revealed a non-linear developmental pattern in network metrics and that most topological changes happen at the late childhood stage (Khundrakpam et al, 2013)

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