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Background: Habenula (HB) function is implicated in substance use disorders and is involved in inhibiting dopamine release in the ventral striatum (VS). While blunted VS reward responsivity is implicated in risk for later substance use, links between HB reinforcement processing and progression of use have not, to our knowledge, been examined among adolescents. In the present study, we longitudinally assessed HB and VS responsivity to social rewards and punishments across adolescence and examined associations with substance use., Methods: Within a longitudinal design, 170 adolescents (53.5% female) completed 1 to 3 functional magnetic resonance imaging scans across 6th to 9th grade and reported yearly substance use across 6th to 11th grade. We examined VS and HB responsivity to social reinforcement during a social incentive delay task in which adolescents received social rewards (smiling faces) and punishments (scowling faces)., Results: We observed increased VS responsivity to social rewards (vs. reward omissions) and increased VS, but decreased HB, responsivity to social punishment avoidance versus receipt. However, contrary to hypotheses, the HB displayed increased responsivity to social rewards (vs. reward omissions). Further, adolescents reporting regular substance use displayed longitudinally declining HB responsivity to social rewards (vs. reward omissions), whereas adolescents reporting no substance use displayed longitudinally increasing HB responsivity. In contrast, whereas VS responsivity to punishment avoidance versus receipt increased longitudinally among regular substance users, it stayed relatively stable among nonusers., Conclusions: These results suggest that differential HB and VS social reinforcement processing trajectories across adolescence are associated with substance use., (Copyright © 2023 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.)

Background: Rates of nonsuicidal self-injury (NSSI) increase dramatically in adolescence. Affective reactivity and adverse social experiences have been linked to NSSI, but less is known about whether these factors may separately or interactively predict NSSI, especially longitudinally. This study combined functional magnetic resonance imaging and a sociometric measure to test whether a combination of neural (e.g., amygdala) reactivity to social punishment and peer-nominated peer acceptance/rejection predicts NSSI longitudinally in adolescence. Amygdala reactivity was examined as a potential neural marker of affective reactivity to social punishment, which may heighten NSSI risk in contexts of social adversity., Methods: One hundred twenty-five adolescents (63 female) completed a social incentive delay task during neuroimaging and school-based peer nominations to measure peer acceptance/rejection. NSSI engagement was assessed at baseline and 1-year follow-up., Results: Greater amygdala reactivity to social punishment predicted greater NSSI engagement 1 year later among adolescents with high peer rejection. This effect for the amygdala was specific to social punishment (vs. reward) and held when controlling for biological sex and pubertal development. Exploratory analyses found that ventral striatum reactivity to social reward and punishment similarly interacted with peer rejection to predict NSSI but that amygdala connectivity with salience network regions did not., Conclusions: Amygdala reactivity to social punishment, in combination with high peer rejection, may increase NSSI risk in adolescence, possibly via heightened affective reactivity to adverse social experiences. Objective measures of neurobiological and social risk factors may improve prediction of NSSI, while therapeutic approaches that target affective reactivity and increase prosocial skills may protect against NSSI in adolescence., (Copyright © 2022 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.)