The Adolescent Functional Connectome is Dynamically Controlled by a Sparse Core of Cognitive and Topological Hubs

Fundamental mechanisms that control the brain’s ability to dynamically respond to cognitive demands are poorly understood, especially during periods of accelerated neural and cognitive maturation, such as adolescence. Using a sparsity-promoting feedback control framework we investigated the controllability of the adolescence functional connectome. Critical feedback costs associated with a region’s control action on itself and the rest of the brain were estimated using resting-state fMRI data from an early longitudinal sample in the Adolescent Brain Cognitive Development (ABCD) study (n = 1394; median (IQR) age = 10.1 (1.1) years at baseline and 12.1 (1.1) years at follow-up). A highly reproducible, core set of predominantly highly connected regions retained their control action over the connectome under high feedback costs. They included posterior visual areas, retrosplenial cortex, cuneus and precuneus, superior parietal lobule, temporal ventral cortex and dorsolateral and lateral prefrontal cortices, i.e., both developed and developing brain regions. These regions were central to the topological organization of the connectome, consistently engaged during spontaneous coordination of resting-state networks, and overlapped with cognitive and topological brain hubs that play ubiquitous roles in cognitive function and the organization of the connectome. Also, most received (integrated) and distributed approximately equal amounts of neural information. These regions’ control action was developmentally stable, i.e., critical feedback costs did not change significantly during puberty, suggesting that, despite ongoing maturation and topological changes in the adolescent brain, fundamental mechanisms of system controllability may be well developed to facilitate information processing and response to cognitive demands.