The Development of Hub Architecture in the Human Functional Brain Network

Abstract

Functional hubs are brain regions that play a crucial role in facilitating communication among parallel, distributed brain networks. The developmental emergence and stability of hubs, however, is not well understood. The current study used measures of network topology drawn from graph theory to investigate the development of functional hubs in 99 participants, 10-20 years of age. We found that hub architecture was evident in late childhood and was stable from adolescence to early adulthood. Connectivity between hub and non-hub ("spoke") regions, however, changed with development. From childhood to adolescence, the strength of connections between frontal hubs and cortical and subcortical spoke regions increased. From adolescence to adulthood, hub-spoke connections with frontal hubs were stable, whereas connectivity between cerebellar hubs and cortical spoke regions increased. Our findings suggest that a developmentally stable functional hub architecture provides the foundation of information flow in the brain, whereas connections between hubs and spokes continue to develop, possibly supporting mature cognitive function.

Developmental Changes in Brain Network Hub Connectivity in Late Adolescence

“…Particularly noteworthy are maturational changes during adolescence, a period that coincides with heightened vulnerability to mental illness and behavioral problems (Paus et al, 2008). Understanding adolescent brain maturation is therefore critical for identifying neurodevelopmental pathways that confer risk or resilience to psychopathology (Di Martino et al, 2014).…”

“…Magnetic resonance imaging (MRI) studies have found that adolescent changes in the organization of large-scale structural and functional neural networks involve the strengthening of long-range connections between distal brain regions (Fair et al, 2007(Fair et al, , 2009Kelly et al, 2009;Dosenbach et al, 2010;Hagmann et al, 2010;Dennis et al, 2013; for review, see Di Martino et al, 2014). Recent studies have suggested that these connections are supported by a collection of spatially distributed and topologically central regions-putative network hubs (Harriger et al, 2012;van den Heuvel et al, 2012;de Reus and van den Heuvel, 2013;van den Heuvel and Sporns, 2013)-and may enhance functional integration (Uddin et al, 2011;Grayson et al, 2014).…”

“…Recent studies have suggested that these connections are supported by a collection of spatially distributed and topologically central regions-putative network hubs (Harriger et al, 2012;van den Heuvel et al, 2012;de Reus and van den Heuvel, 2013;van den Heuvel and Sporns, 2013)-and may enhance functional integration (Uddin et al, 2011;Grayson et al, 2014). The maturation of connectivity between hub regions may thus enable the integrated brain function that marks the transition from adolescent to adult patterns of neural activity (Fair et al, 2009).…”

“…Despite this view, recent evidence also suggests that hub-hub connectivity may be established early in development, with most subsequent developmental change occurring in connections between hubs and topologically peripheral nonhub regions (Hwang et al, 2013;Towlson et al, 2013). For example, one recent study of preterm born infants found that strong connectivity between a core set of hub regions, referred to as a "rich club" van den Heuvel and Sporns, 2011), was present by 30 weeks of gestation, and remained relatively stable until term-equivalent age (Ball et al, 2014).…”

Emergence of system roles in normative neurodevelopment

“…Network modularity, a measure of the segregation between modules, is high during young adulthood and decreases across the latter life span (6,7). Other features of network reorganization accompany development (8), including a growing preference for interactions between hubs and nonhubs (9), and between regions separated by large physical distances (10).…”