Protracted prediction: Neurodevelopment of reward processing in the adolescent cerebellum.

Abstract

Adolescence is characterized by heightened reward sensitivity and risky decision-making. Prevailing neurodevelopmental frameworks attribute these behavioral trends to a maturational imbalance between rapidly developing motivational brain regions, and slower-maturing prefrontal cognitive control circuitry. However, these models overlook the cerebellum-a structure that demonstrates protracted development across adolescence and reciprocal connectivity with both striatum and prefrontal cortex. Here, we conducted a systematic literature search and activation likelihood estimation (ALE) meta-analysis of functional magnetic resonance imaging (fMRI) studies examining reward anticipation and feedback processing in healthy adolescents (19 studies; 55 cerebellar peaks). In adults, a recent ALE analysis found a diffuse set of cognitive and affective cerebellar regions is recruited during reward anticipation, while feedback-locked activation is circumscribed and mostly restricted to the Vermis (Kruithof et al., 2023). In adolescents, we found evidence for a reward phase-specific spatial dissociation relative to adults. In adolescents, reward anticipation-locked activity is restricted to regions of the Vermis that are functionally connected to occipital and salience networks. Conversely, feedback processing elicits diffuse activation across bilateral Crus I/II regions that are connected to frontoparietal, default-mode, and limbic networks. These results suggest a proactive engagement of cortico-cerebellar networks during reward anticipation in adults, and a reactive recruitment of cortico-cerebellar networks post-feedback in adolescents. Adolescents may have less mature internal models for optimizing decision-making, and as a result they may require more widespread recruitment of cortico-cerebellar cognitive and affective circuitry post-feedback. Prevailing maturational imbalance models of youth decision-making should be expanded to incorporate developmental changes in cerebellar reward processing.