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Interdependent Neural Correlates of Reward and Punishment Sensitivity During Rewarded Action and Inhibition of Action.

ABSTRACT: Imaging studies have distinguished the brain correlates of approach and avoidance behaviors and suggested the influence of individual differences in trait sensitivity to reward (SR) and punishment (SP) on these neural processes. Theoretical work of reinforcement sensitivity postulates that SR and SP may interdependently regulate behavior. Here, we examined the distinct and interrelated neural substrates underlying rewarded action versus inhibition of action in relation to SR and SP as evaluated by the Sensitivity to Punishment and Sensitivity to Reward Questionnaire. Forty-nine healthy adults performed a reward go/no-go task with approximately 2/3 go and 1/3 no-go trials. Correct go and no-go responses were rewarded and incorrect responses were penalized. The results showed that SR and SP modulated rewarded go and no-go, respectively, both by recruiting the rostral anterior cingulate cortex and left middle frontal gyrus (rACC/left MFG). Importantly, SR and SP influenced these regional activations in opposite directions, thus exhibiting an antagonistic relationship as suggested by the reinforcement sensitivity theory. Furthermore, mediation analysis revealed that heightened SR contributed to higher rewarded go success rate via enhanced rACC/left MFG activity. The findings demonstrate interrelated neural correlates of SR and SP to support the diametric processes of behavioral approach and avoidance.

SUBMITTER: Le TM

PROVIDER: S-EPMC7132903 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Interdependent Neural Correlates of Reward and Punishment Sensitivity During Rewarded Action and Inhibition of Action.

Le Thang M TM Wang Wuyi W Zhornitsky Simon S Dhingra Isha I Zhang Sheng S Li Chiang-Shan R CR

Cerebral cortex (New York, N.Y. : 1991) 20200301 3

Imaging studies have distinguished the brain correlates of approach and avoidance behaviors and suggested the influence of individual differences in trait sensitivity to reward (SR) and punishment (SP) on these neural processes. Theoretical work of reinforcement sensitivity postulates that SR and SP may interdependently regulate behavior. Here, we examined the distinct and interrelated neural substrates underlying rewarded action versus inhibition of action in relation to SR and SP as evaluated ...[more]

PMID: 31667492

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Project description:Risk for substance use disorder (SUD) is associated with poor response inhibition and heightened reward sensitivity. During adolescence, incentives improve performance on response inhibition tasks and increase recruitment of cortical control areas (Geier et al., 2010) associated with SUD (Chung et al., 2011). However, it is unknown whether incentives moderate the relationship between response inhibition and trait-level psychopathology and personality features of substance use risk. We examined these associations in the current project using a rewarded antisaccade (AS) task (Geier et al., 2010) in youth at risk for substance use. Participants were 116 adolescents and young adults (ages 12-21) from the University of Pittsburgh site of the National Consortium on Adolescent Neurodevelopment and Alcohol [NCANDA] study, with neuroimaging data collected at baseline and 1 year follow up visits. Building upon previous work using this task in normative developmental samples (Geier et al., 2010) and adolescents with SUD (Chung et al., 2011), we examined both trial-wise BOLD responses and those associated with individual task-epochs (cue presentation, response preparation, and response) and associated them with multiple substance use risk factors (externalizing and internalizing psychopathology, family history of substance use, and trait impulsivity). Results showed that externalizing psychopathology and high levels of trait impulsivity (positive urgency, SUPPS-P) were associated with general decreases in antisaccade performance. Accompanying this main effect of poor performance, positive urgency was associated with reduced recruitment of the frontal eye fields (FEF) and inferior frontal gyrus (IFG) in both a priori regions of interest and at the voxelwise level. Consistent with previous work, monetary incentive improved antisaccade behavioral performance and was associated with increased activation in the striatum and cortical control areas. However, incentives did not moderate the association between response inhibition behavioral performance and any trait-level psychopathology and personality factor of substance use risk. Reward interactions were observed for BOLD responses at the task-epoch level, however, they were inconsistent across substance use risk types. The results from this study may suggest poor response inhibition and heightened reward sensitivity are not overlapping neurocognitive features of substance use risk. Alternatively, more subtle, common longitudinal processes might jointly explain reward sensitivity and response inhibition deficits in substance use risk.

Project description:ObjectiveRecent findings suggest that diminished processing of positive contextual information about others during interactions may contribute to social impairment in the schizophrenia spectrum. This could be due to general social context processing deficits or specific biases against positive information. We studied the impact of positive and negative social contextual information during social interactions using functional neuroimaging and probed whether these neural mechanisms were associated with real-life social functioning in schizophrenia spectrum disorders.MethodsPatients with a schizophrenia spectrum disorder (N = 23) and controls disorder (N = 25) played three multi-round trust games during functional magnetic resonance imaging scanning, with no, positive and negative information about the counterpart's trustworthiness, while all counterparts were programmed to behave trustworthy. The main outcome variable was the height of the shared amount in the trust game, i.e. investment, representing an indication of trust. The first investment in the game was considered to be basic trust, since no behavioural feedback was given yet. We performed region-of-interest analyses and examined the association with real-life social functioning using the experience sampling method.ResultsSocial contextual information had no effect on patients' first investments, whereas controls made the lowest investment after negative and the highest investments after positive contextual information was provided. Over trials, patients decreased investments, suggesting reduced social reward learning, whereas controls increased investments in response to behavioural feedback in the negative context. Patients engaged the dorsolateral prefrontal cortex less than controls during context presentation and showed reduced activity within the caudate during repayments. In patients, lower investments were associated with more time spent alone and social exclusion and lower caudate activation was marginally significantly associated with higher perceived social exclusion.ConclusionThe failure to adapt trust to positive and negative social contexts suggests that patients have a general insensitivity to prior social information, indicating top-down processing impairments. In addition, patients show reduced sensitivity to social reward, i.e. bottom-up processing deficits. Moreover, lower trust and lower neural activation were related to lower real-life social functioning. Together, these findings indicate that improving trust and social interactions in schizophrenia spectrum needs a multi-faceted approach that targets both mechanisms.

Dataset Information

Interdependent Neural Correlates of Reward and Punishment Sensitivity During Rewarded Action and Inhibition of Action.

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Interdependent Neural Correlates of Reward and Punishment Sensitivity During Rewarded Action and Inhibition of Action.

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