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

Wyngaarden, James B; Johnston, Camille; Sazhin, Daniel; Dennison, Jeffrey B.; Zaff, Ori; Fareri, Dominic S.; McCloskey, Michael; Alloy, Lauren B.; Smith, David V.; Jarcho, Johanna M.

doi:10.1101/2023.01.17.524305

Cited by 3 publications

(3 citation statements)

References 118 publications

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“…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.…”

Section: Discussionmentioning

confidence: 99%

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

Sazhin,

Wyngaarden,

Dennison

et al. 2023

Preprint

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Many decisions happen in social contexts such as negotiations, yet little is understood about how people balance fairness versus selfishness. Past investigations found that activation in brain areas involved in executive function and reward processing was associated with people offering less with no threat of rejection from their partner, compared to offering more when there was a threat of rejection. However, it remains unclear how trait reward sensitivity may modulate activation and connectivity patterns in these situations. To address this gap, we used task-based fMRI to examine the relation between reward sensitivity and the neural correlates of bargaining choices. Participants (N = 54) completed the Sensitivity to Punishment (SP)/Sensitivity to Reward (SR) Questionnaire and the Behavioral Inhibition System/Behavioral Activation System scales. Participants performed the Ultimatum and Dictator Games as proposers and exhibited strategic decisions by being fair when there was a threat of rejection, but being selfish when there was not a threat of rejection. We found that strategic decisions evoked activation in the Inferior Frontal Gyrus (IFG) and the Anterior Insula (AI). Next, we found elevated IFG connectivity with the Temporoparietal junction (TPJ) during strategic decisions. Finally, we explored whether trait reward sensitivity modulated brain responses while making strategic decisions. We found that people who scored lower in reward sensitivity made less strategic choices when they exhibited higher AI-Angular Gyrus connectivity. Taken together, our results demonstrate how trait reward sensitivity modulates neural responses to strategic decisions, potentially underscoring the importance of this factor within social and decision neuroscience.

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Section: Discussionmentioning

confidence: 99%

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

Sazhin,

Wyngaarden,

Dennison

et al. 2023

Preprint

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“…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.…”

Section: Discussionmentioning

confidence: 99%

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

Wang,

Chang,

Liou

et al. 2024

Psychophysiology

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Unselfishness is admired, especially when collaborations between groups of various scales are urgently needed. However, its neural mechanisms remain elusive. In a tri‐MRI dyad‐hyperscanning experiment involving 26 groups, each containing 4 participants as two rotating pairs in a coordination game, we sought to achieve reciprocity, or “winning in turn by the two interacting players,” as the precursor to unselfishness. Due to its critical role in social processing, the right temporal–parietal junction (rTPJ) was the seed for both time domain (connectivity) and frequency domain (i.e., coherence) analyses. For the former, negative connectivity between the rTPJ and the mentalizing network areas (e.g., the right inferior parietal lobule, rIPL) was identified, and such connectivity was further negatively correlated with the individual's final gain, supporting our task design that “rewarded” the reciprocal participants. For the latter, cerebral coherences of the rTPJs emerged between the interacting pairs (i.e., within‐group interacting pairs), and the coupling between the rTPJ and the right superior temporal gyrus (rSTG) between the players who were not interacting with each other (i.e., within‐group noninteracting pairs). These coherences reinforce the hypotheses that the rTPJ–rTPJ coupling tracks the collaboration processes and the rTPJ–rSTG coupling for the emergence of decontextualized shared meaning. Our results underpin two social roles (inferring others’ behavior and interpreting social outcomes) subserved by the rTPJ‐related network and highlight its interaction with other‐self/other‐concerning brain areas in reaching co‐benefits among unselfish players.

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“…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.…”

Section: Discussionmentioning

confidence: 99%

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

Sazhin,

Dachs,

Smith

2023

Preprint

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Explore-exploit research has challenges in generalizability due to a limited theoretical basis of exploration and exploitation. Neuroimaging can help identify whether explore-exploit decisions use an opponent processing system to address this issue. Thus, we conducted a coordinate-based meta-analysis (N=23 studies) where we found activation in the dorsal lateral prefrontal cortex and anterior cingulate cortex during exploration versus exploitation, providing some evidence for opponent processing. However, the conjunction of explore-exploit decisions was associated with activation in the dorsal anterior cingulate cortex, dorsal medial prefrontal cortex, and anterior insula, suggesting that these brain regions do not engage in opponent processing. Further, exploratory analyses revealed heterogeneity in brain responses between task types during exploration and exploitation respectively. Coupled with results suggesting that activation in exploration and exploitation decisions is generally more similar than it is different suggests there remain significant challenges toward characterizing explore-exploit decision making. Nonetheless, dlPFC and ACC activation differentiate explore and exploit decisions and identifying these responses can help in targeted interventions aimed at manipulating these decisions.

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

Cited by 3 publications

References 118 publications

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

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

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

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

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