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. 163 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 (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 executive function areas were associated with improved executive function, 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 executive function.Significance Statement Anatomical studies in nonhuman primates demonstrate that frontostriatal circuits are essential for integration of neural functions underlying reward processing and cognition, with human neuroimaging studies linking alterations in these circuits to psychopathology. The present study characterized the developmental trajectories of frontostriatal resting state networks from childhood to young adulthood. We demonstrate that ventral and dorsal aspects of the striatum exhibit distinct age-related changes that predicted developmental improvements in reward-related decision making and executive function. These results highlight that adolescence is characterized by distinct changes in frontostriatal networks that may relate to normative increases in risk-taking. Atypical developmental trajectories of frontostriatal networks may contribute to adolescent-onset psychopathology.