Paper

Corticostriatal responses to social reward are linked to reward sensitivity and subclinical substance use

Sazhin, Daniel, Alloy, Lauren B, Fareri, Dominic, Dennison, Jeffrey B, Johnston, Camille R, Wyngaarden, James B, Mccloskey, Michael, Jarcho, Johanna M, Zaff, Ori, Smith, David V

2024

Overview

Aberrant levels of reward sensitivity have been linked to substance use disorder and are characterized by alterations in reward processing in the ventral striatum (VS). Less is known about how reward sensitivity and subclinical substance use relate to striatal function during social rewards (e.g., positive peer feedback). Testing this relation is critical for predicting risk for development of substance use disorder. In this pre-registered study, participants (N=44) underwent fMRI while completing well-matched tasks that assess neural response to reward in social and monetary domains. Contrary to our hypotheses, aberrant reward sensitivity blunted the relationship between substance use and striatal activation during receipt of rewards, regardless of domain. Moreover, exploratory whole-brain analyses showed unique relations between substance use and social rewards in temporoparietal junction. Psychophysiological interactions demonstrated that aberrant reward sensitivity is associated with increased connectivity between the VS and ventromedial prefrontal cortex during social rewards. Finally, we found that substance use was associated with decreased connectivity between the VS and dorsomedial prefrontal cortex for social rewards, independent of reward sensitivity. These findings demonstrate nuanced relations between reward sensitivity and substance use, even among those without substance use disorder, and suggest altered reward-related engagement of cortico-VS responses as potential predictors of developing disordered behavior.Competing Interest StatementThe authors have declared no competing interest.Footnotes* We have updated this document in response to clear and thoughtful feedback from reviewers on the original manuscript. In this revised document, major changes center on clarifying the hypotheses and overarching goals, adding detail and consistency to our discussion of subclinical substance use as it is operationalized here, and clarifying interpretations of our results. We believe that these changes have improved the overall quality of the manuscript.* https://openneuro.org/datasets/ds004920/versions/1.1.0

• Publisher: Cold Spring Harbor Laboratory Press
• Subject: Brain mapping / Drug use / Functional magnetic resonance imaging / Neostriatum / Neural networks / Prefrontal cortex / Reinforcement / Risk factors / Substance use