Neural responses to reward valence and magnitude from pre- to early adolescence

• Published in: NeuroImage (Orlando, Fla.) Fla.), 2023-07, Vol.275, p.120166-120166, Article 120166
• Main Authors: Gadassi Polack, Reuma, Mollick, Jessica A., Keren, Hanna, Joormann, Jutta, Watts, Richard
• Format: Article
• Language: English
• Subjects: ABCD study; Adolescence; Adolescents; Age groups; Brain - physiology; Brain architecture; Brain Mapping; Brain research; Child; Child development; Cognitive ability; Corpus Striatum - physiology; Feedback; Functional anatomy; Functional magnetic resonance imaging; Humans; Incentives; Information processing; Longitudinal studies; Magnetic Resonance Imaging; Monetary incentive delay task; Motivation; Neostriatum; Prefrontal Cortex; Reinforcement; Reward; Reward processing; Teenagers; Young adults
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2023.120166

·Brain regions mostly encode incentive valence or magnitude during reward processing.·This encoding specialization is highly consistent from pre to early adolescence.·Brain regions’ encoding specialization changes with reward processing phase.·Neural reactivity during success feedback increased from pre to early adolescence.·Success feedback reactivity increases were in prefrontal and subcortical regions. Neural activation during reward processing is thought to underlie critical behavioral changes that take place during the transition to adolescence (e.g., learning, risk-taking). Though literature on the neural basis of reward processing in adolescence is booming, important gaps remain. First, more information is needed regarding changes in functional neuroanatomy in early adolescence. Another gap is understanding whether sensitivity to different aspects of the incentive (e.g., magnitude and valence) changes during the transition into adolescence. We used fMRI from a large sample of preadolescent children to characterize neural responses to incentive valence vs. magnitude during anticipation and feedback, and their change over a period of two years. Data were taken from the Adolescent Cognitive and Brain DevelopmentSM (ABCD®) study release 3.0. Children completed the Monetary Incentive Delay task at baseline (ages 9–10) and year 2 follow-up (ages 11–12). Based on data from two sites (N = 491), we identified activation-based Regions of Interest (ROIs; e.g., striatum, prefrontal regions, etc.) that were sensitive to trial type (win $5, win $0.20, neutral, lose $0.20, lose $5) during anticipation and feedback phases. Then, in an independent subsample (N = 1470), we examined whether these ROIs were sensitive to valence and magnitude and whether that sensitivity changed over two years. Our results show that most ROIs involved in reward processing (including the striatum, prefrontal cortex, and insula) are specialized, i.e., mainly sensitive to either incentive valence or magnitude, and this sensitivity was consistent over a 2-year period. The effect sizes of time and its interactions were significantly smaller (0.002≤η2≤0.02) than the effect size of trial type (0.06≤η2≤0.30). Interestingly, specialization was moderated by reward processing phase but was stable across development. Biological sex and pubertal status differences were few and inconsistent. Developmental changes were mostly evident during success feedback, where neural reactivity increased over time