Frontostriatal Networks Undergo Functional Specialization during Adolescence That Follows a Ventral–Dorsal Gradient: Developmental Trajectories and Longitudinal Associations

Abstract

Seminal studies in animal neuroscience demonstrate that frontostriatal circuits exhibit a ventral–dorsal functional gradient to integrate neural functions related to reward processing and cognitive control. Prominent neurodevelopmental models posit that heightened reward seeking and risk taking during adolescence result from maturational imbalances between frontostriatal neural systems underlying reward processing and cognitive control. The present study investigated whether the development of ventral (VS) and dorsal (DS) striatal resting-state connectivity (rsFC) networks along this proposed functional gradient relates to putative imbalances between reward and executive systems posited by a dual neural systems theory of adolescent development. One hundred sixty-three participants aged 11–25 years (54% female, 90% white) underwent resting scans at baseline and biennially thereafter, yielding 339 scans across four assessment waves. We observed developmental increases in VS rsFC with brain areas implicated in reward processing (e.g., subgenual cingulate gyrus and medial orbitofrontal cortex) and concurrent decreases with areas implicated in executive function (EF; e.g., ventrolateral and dorsolateral prefrontal cortices). DS rsFC exhibited the opposite pattern. More rapid developmental increases in VS rsFC with reward areas were associated with developmental improvements in reward-based decision-making, whereas increases in DS rsFC with EF areas were associated with improved EF, though each network exhibited some crossover in function. Collectively, these findings suggest that typical adolescent neurodevelopment is characterized by a divergence in ventral and dorsal frontostriatal connectivity that may relate to developmental improvements in affective decision-making and EF.