Abstract

Late human development is characterized by the maturation of high-level functional processes, which rely on reshaping of white matter connections, as well as synaptic density. However, the relationship between the whole-brain dynamics and the underlying white matter networks in neurodevelopment is largely unknown. In this study, we focused on how the structural connectome shapes the emerging dynamics of cerebral development between the ages of 6 and 33 years, using functional and diffusion magnetic resonance imaging combined into a spatiotemporal connectivity framework. We defined two new measures of brain dynamics, namely the system diversity and the spatiotemporal diversity, which quantify the level of integration/segregation between functional systems and the level of temporal self-similarity of the functional patterns of brain dynamics, respectively. We observed a global increase in system diversity and a global decrease and local refinement in spatiotemporal diversity values with age. In support of these findings, we further found an increase in the usage of long-range and inter-system white matter connectivity and a decrease in the usage of short-range connectivity with age. These findings suggest that dynamic functional patterns in the brain progressively become more integrative and temporally self-similar with age. These functional changes are supported by a greater involvement of long-range and inter-system axonal pathways.

Highlights

  • Human brain development from childhood to the early adult stage is marked by maturation of high-level brain processes, such as cognitive control, executive functions, and multimodal integration (Burr & Gori, 2012; Goswami, 2011)

  • We associated with every brain region a functional system (FS) as defined by Yeo et al (2011): visual (VIS), somato-motor (SM), dorsal attention (DA), ventral attention (VA), limbic (LIM), frontoparietal (FP), and default mode (DM) systems

  • We defined two novel measures—namely, the spatiotemporal diversity (STD) and the system diversity (SD)—to characterize the functional system dynamic recruitment and temporal self-similarity of the different connected components (CCs) (Figure 1C). Both measures were compared between two age groups—adults and children—across three different spatial scales of investigation: global, functional system level, and nodal level

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Summary

Introduction

Human brain development from childhood to the early adult stage is marked by maturation of high-level brain processes, such as cognitive control, executive functions, and multimodal integration (Burr & Gori, 2012; Goswami, 2011) These processes arise through integration of information from local functional systems within complex neural networks, whose development is achieved through the optimization of white matter axonal bundles, as well as the selection of local connections at the neuronal level (i.e., synaptic pruning; Tau & Peterson, 2010). Network neuroscience serves as an ideal candidate to represent these relations in terms of brain static functional connectivity (FC), structural connectivity (SC), and, recently, dynamic functional connectivity (dFC) Both structural connectivity and functional connectivity have been widely studied (Collin & van den Heuvel, 2013). How dynamic functional connectivity patterns evolve with structural connections across neurodevelopment remains largely unknown

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