Modular Segregation of Structural Brain Networks Supports the Development of Executive Function in Youth

Abstract

SUMMARY The human brain is organized into large-scale functional modules that have been shown to evolve in childhood and adolescence. However, it remains unknown whether the underlying white matter architecture is similarly refined during development, potentially allowing for improvements in executive function. In a sample of 882 participants (ages 8–22) who underwent diffusion imaging as part of the Philadelphia Neurodevelopmental Cohort, we demonstrate that structural network modules become more segregated with age, with weaker connections between modules and stronger connections within modules. Evolving modular topology facilitates global network efficiency, and is driven by age-related strengthening of hub edges present both within and between modules. Critically, both modular segregation and network efficiency are associated with enhanced executive performance, and mediate the improvement of executive functioning with age. Together, results delineate a process of structural network maturation that supports executive function in youth.

A three‐wave longitudinal study of subcortical–cortical resting‐state connectivity in adolescence: Testing age‐ and puberty‐related changes

“…Together, these findings may be interpreted as change in local versus distributed networks in which specific functional networks both strengthen and weaken across adolescence. Previous work also showed that structural networks become more segregated across development (Baum, Ciric, Roalf, Betzel, et al, ), and that BOLD dimensionality decreases with age (Kundu et al, ). One suggested interpretation is that these changes may maximize the neural efficiency of interregional communication (Stevens, ).…”

“…These findings fit prior research that has shown strengthening of functional connectivity in cortico-cortical connections (Supekar, Musen, & Menon, 2009), as well as subcortico-subcortical connectivity (van Duijvenvoorde, Achterberg, et al, 2016), and extend previous findings by providing longitudinal evidence for stronger integration within subcortical and Together, these findings may be interpreted as change in local versus distributed networks in which specific functional networks both strengthen and weaken across adolescence. Previous work also showed that structural networks become more segregated across development (Baum, Ciric, Roalf, Betzel, et al, 2017), and that BOLD dimensionality decreases with age (Kundu et al, 2018). One suggested interpretation is that these changes may maximize the neural efficiency of interregional communication (Stevens, 2016).…”

Charting shared developmental trajectories of cortical thickness and structural connectivity in childhood and adolescence

“…This modular organisation is supported by evidence that cortical regions can be defined based on the extent of their shared anatomical connections (Bullmore & Sporns, 2012;Hilgetag, Burns, O'Neill, Scannell, & Young, 2000). Both neuronal density and dendritic spine density are correlated to areal connectivity (Beul & Hilgetag, 2019;Scholtens, Schmidt, de Reus, & van den MP, 2014), and white matter networks derived from MRI can similarly be split in subnetworks of connections, or modules, that appear to support known cortical systems, vary together with age and can be disrupted in neurodevelopmental disorder Baum et al, 2017;Faskowitz, Yan, Zuo, & Sporns, 2018). Therefore, macroscopic markers of brain development, including cortical thickness and measures of white matter connectivity reflect regionally-varying patterns of complex, interlinked microscopic processes across the white and grey matter.…”

“…Studies using diffusion MRI have shown markers of tissue organisation, including fractional anisotropy (FA), increase with age during childhood (Lebel, Walker, Leemans, Phillips, & Beaulieu, 2008), with maturation of commissural and projection fibres regions preceding intrahemispheric association fibres (Lebel & Beaulieu, 2011). The effects of white matter maturation on structural connectivity measures reveal large-scale topological organisation of the structural connectome with measures of network efficiency and modularity increasing over childhood and adolescence (Baum et al, 2017;Zhao et al, 2015).…”

Adolescent Tuning of Association Cortex in Human Structural Brain Networks

“…However, Chen et al (2013) reported increases in the number of streamlines and edge density from childhood (5 years) to adulthood (30 years). Recently, Baum et al (2017) reported increases in within-module connectivity, and decreases in between-module connectivity in tractography-derived white matter networks. While tractography-derived structural connectomes show some overlap with structural correlation networks (Gong et al 2012), interpretation of developmental changes in white-matter connectivity relative to development of structural correlations will require concurrent studies of both modalities in the same datasets.…”