Corticostriatal Responses to Social Reward are Linked to Trait Reward Sensitivity and Subclinical Substance Use in Young Adults

Abstract

Substance use (SU) has been linked to alterations in reward processing in the ventral striatum (VS). However, less is known about how SU relates to striatal activation and connectivity during social rewards (e.g., positive peer feedback). In this pre-registered study, we hypothesized that SU would be associated with activation and functional connectivity of the VS during receipt of social rewards. Participants (N=44) underwent two fMRI tasks to isolate neural response to social and monetary rewards. The tasks involved choosing between two stimuli: either two purported peers, with the goal of identifying the peer who liked the participant (social); or two doors, with the goal of identifying the door containing a $0.50 prize (monetary). We predicted that VS activation in response to social rewards would be correlated with SU, independent of reward sensitivity (RS); however, an exploratory whole-brain analysis revealed SU was related to activation in the temporoparietal junction instead. Moreover, results showed that aberrant RS blunts the relationship between SU and striatal activation during receipt of rewards, regardless of their domain. Psychophysiological interaction (PPI) analysis demonstrated that SU was associated with decreased connectivity between the VS and dorsomedial prefrontal cortex for social rewards, independent of RS. Exploratory analyses further revealed that RS is associated with increased connectivity between the VS and ventromedial prefrontal cortex during social rewards. Taken together, these findings shed light on the relationships between potential risk factors for developing substance use disorder.

Trait Reward Sensitivity Modulates Connectivity with the Temporoparietal Junction and Anterior Insula during Strategic Decision Making

“…These results provide greater insights into how reward processes interact with social decisions, involving brain processes that appraise the roles of other people while making choices. Since aberrant reward sensitivity is a major mechanism in substance use and depressive and bipolar disorders, investigating how reward sensitivity modulates brain processes during social contexts could provide considerably more understanding into how people make maladaptive decisions resulting in substance use (Bart et al, 2021; Heilig et al, 2016; Wyngaarden et al, 2023). Such work could help identify people at risk for substance use disorders and help develop interventions for people with aberrant reward patterns.…”

When “more for others, less for self” leads to co‐benefits: A tri‐MRI dyad‐hyperscanning study

“…Even for the latest study by Wyngaarden et al. (2023), who tried to parameterize the effect of social reward vs. monetary win/loss, the ROIs still lie in the same NAcc, mPFC, among other ROIs. This inherent limitation that in realistic decision‐making contexts, both social and monetary factors naturally co‐occur, may not be easy to separate the contribution from either social or monetary rewards alone.…”

Meta-Analysis Reveals That Explore-Exploit Decisions are Dissociable by Activation in the Dorsal Lateral Prefrontal Cortex, Anterior Insula, and the Anterior Cingulate Cortex

“…Brain responses may be modulated by substance use and mediated by social context (Sazhin et al 2020). Sharing rewards with friends decreased connectivity between VS and dorsomedial prefrontal cortex (Wyngaarden et al 2023), suggesting that social contexts are an important feature of understanding substance use decisions. Future investigation could also study the role of trends in decision making and assess whether substance users forecast future trends worse than non-substance users.…”