Corticostriatal responses to social reward are linked to trait reward sensitivity and subclinical substance use in young adults.

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.

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

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.

Social feedback biases emerge during recall but not prediction and shift across the development of social anxiety.

Memory is a reconstructive process that can result in events being recalled as more positive or negative than they actually were. While positive recall biases may contribute to well-being, negative recall biases may promote internalizing symptoms, such as social anxiety. Adolescence is characterized by increased salience of peers and peak incidence of social anxiety. Symptoms often wax and wane before becoming more intractable during adulthood. Open questions remain regarding how and when biases for social feedback are expressed and how individual differences in biases may contribute to social anxiety across development. Two studies used a social feedback and cued response task to assess biases about being liked or disliked when retrieving memories vs. making predictions. Findings revealed a robust positivity bias about memories for social feedback, regardless of whether memories were true or false. Moreover, memory bias was associated with social anxiety in a developmentally sensitive way. Among adults (study 1), more severe symptoms of social anxiety were associated with a negativity bias. During the transition from adolescence to adulthood (study 2), age strengthened the positivity bias in those with less severe symptoms and strengthened the negativity bias in those with more severe symptoms. These patterns of bias were isolated to perceived memory retrieval and did not generalize to predictions about social feedback. These results provide initial support for a model by which schemas may infiltrate perceptions of memory for past, but not predictions of future, social events, shaping susceptibility for social anxiety, particularly during the transition into adulthood.

Substance Abuse in Emerging Adults: The Role of Neuromelanin and Ventral Striatal Response to Social and Monetary Rewards.

Perturbations in dopamine system function may increase risk of substance use disorder (SUD). We recently demonstrated that neuromelanin (NM) MRI signal in the substantia nigra, a non-invasive index of dopamine system function, is elevated in long term cocaine users (Cassidy et al., 2020). However, it is unclear whether elevated NM-MRI signal is linked to risk of SUD, or is a byproduct of long-term drug use. Our prior work failed to show relations between NM-MRI signal and functional engagement of ventral striatum during a monetary reward task. However, social experiences are commonly linked to drug use and relapse. Given that, NM-MRI signal may be more closely linked to ventral striatal engagement during social, rather than monetary reward processing. Emerging adults (n = 33, 21.88 ± 4.35 years) with varying levels of substance abuse, but without SUD, underwent NM-MRI and fMRI during social and monetary reward processing tasks. Voxelwise analysis within the substantia nigra (SN) demonstrated lower NM-MRI signal was associated with more severe substance abuse. Lower right ventral striatal engagement to social reward was also associated with more severe substance abuse. This relation was moderated by SN NM-MRI signal such that diminished striatal response to reward was associated with greater substance abuse among those with low NM-MRI signal, but lower substance abuse among those with high NM-MRI signal. Unexpectedly, higher right ventral striatal engagement during monetary reward was associated with more severe substance abuse. This relation was moderated by SN NM-MRI signal such that greater striatal response to reward was associated with greater substance abuse among those with low NM-MRI signal. Taken together, we provide preliminary evidence that, in emerging adults, low rather than high dopamine system function may increase risk of substance abuse, and strengthen the association between substance use and the brain's sensitivity to social and monetary outcomes in different ways.

The Role of Social Reward and Corticostriatal Connectivity in Substance Use.

This report describes an ongoing R03 grant that explores the links between trait reward sensitivity, substance use, and neural responses to social and nonsocial reward. Although previous research has shown that trait reward sensitivity and neural responses to reward are linked to substance use, whether this relationship is impacted by how people process social stimuli remains unclear. We are investigating these questions via a neuroimaging study with college-aged participants, using individual difference measures that examine the relation between substance use, social context, and trait reward sensitivity with tasks that measure reward anticipation, strategic behavior, social reward consumption, and the influence of social context on reward processing. We predict that substance use will be tied to distinct patterns of striatal dysfunction. Specifically, reward hyposensitive individuals will exhibit blunted striatal responses to social and non-social reward and enhanced connectivity with the orbitofrontal cortex; in contrast, reward hypersensitive individuals will exhibit enhanced striatal responses to social and non-social reward and blunted connectivity with the orbitofrontal cortex. We also will examine the relation between self-reported reward sensitivity, substance use, and striatal responses to social reward and social context. We predict that individuals reporting the highest levels of substance use will show exaggerated striatal responses to social reward and social context, independent of self-reported reward sensitivity. Examining corticostriatal responses to reward processing will help characterize the relation between reward sensitivity, social context and substance use while providing a foundation for understanding risk factors and isolating neurocognitive mechanisms that may be targeted to increase the efficacy of interventions.