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Smith, D. V.

Publications and source records attributed to Smith, D. V..

At least 19 recordsLinked to original sources

Associations Between Neural Responses to Social Fairness and Financial Exploitation Vulnerability Vary With Age and Emotional Intelligence

Financial exploitation often arises in social contexts in which individuals must evaluate fairness, trust, and interpersonal information during financial decisions. We examined whether neural responses to fairness in social versus nonsocial contexts relate to financial exploitation vulnerability and whether these relationships vary with age, emotional intelligence, and affect. A total of 310 adults spanning ages 21-89 completed an fMRI Ultimatum Game in which they accepted or rejected offers from human and computer partners, along with measures of financial exploitation vulnerability, emotional intelligence, and affect. Participants were strongly sensitive to offer fairness, and individual differences in behavioral sensitivity to partner type were associated with social-relative anterior insula responses to unfairness. Greater baseline negative affect was associated with stronger anterior insula differentiation between social and nonsocial fairness. Financial exploitation vulnerability was associated with prefrontal responses to social-relative fairness in ways that depended on individual characteristics: age moderated its association with dorsomedial prefrontal cortex activation, whereas emotional intelligence moderated its association with dorsolateral prefrontal cortex activation. Whole-brain connectivity analyses further showed that age moderated associations between emotional intelligence and executive control network connectivity with posterior cingulate and right temporoparietal regions. These findings suggest that vulnerability to financial exploitation is reflected in how social context is integrated with affective and individual characteristics across adulthood.

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Differences in other-directed emotion regulation tracks connectivity between amygdala and prefrontal regions during fairness decisions

Fairness decisions often integrate affective responses within a social context, yet emotion regulation in this literature has been largely studied as a self-directed process rather than an interpersonal one. We examined how individual differences in other-directed emotion regulation--measured with the Emotion Regulation of Others and Self (EROS) scale--relate to behavioral and neural responses during fairness decisions in 138 adults completing a variant of the Ultimatum Game with human and computer partners during fMRI. Behaviorally, participants who more strongly endorsed worsening others emotions rejected unfair offers more frequently, and this tendency interacted with offer fairness to amplify rejection of unfair offers. At the neural level, the left anterior insula tracked offer unfairness more strongly in social versus nonsocial contexts, consistent with sociality modulating the neural encoding of fairness. Right dlPFC activation during socially unfair offers was greater among individuals who preferred to improve others emotions. Connectivity analyses revealed that social fairness sensitivity predicted stronger amygdala-orbitofrontal and amygdala-dmPFC coupling; the latter was further amplified among individuals higher in other-directed emotion worsening. Together, these findings identify interpersonal emotion regulation as an understudied source of variation in the affective and prefrontal systems supporting fairness-based social decisions.

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Striatal Social Reward Sensitivity Predicts Trust-Related Brain Responses Depending on Closeness and Depression

BackgroundDepression is associated with social dysfunction, but the mechanisms linking affective symptoms to disrupted close relationships remain poorly understood. One possibility is that depression alters how people experience rewards shared with close others and how they interpret partners actions. It remains unclear whether neural sensitivity to shared reward predicts social valuation during more complex interactions such as reciprocated trust. MethodsIn this preregistered fMRI study, participants completed a reward-sharing task and a Trust Game with a close friend, a stranger, and a computer. We measured striatal shared reward sensitivity (SRS; friend > computer) and tested whether it related to subsequent investment behavior and brain responses to trust reciprocation. Depressive symptoms and perceived closeness were assessed via self-report. ResultsIn a final sample of n = 123, participants reporting more depressive symptoms invested more in their friend than in the computer. Striatal SRS predicted temporoparietal junction responses to reciprocated trust, but this association depended jointly on social closeness and depression -- with depression reversing the expected pattern among individuals reporting closer relationships. Striatal SRS was also inversely associated with connectivity between the default mode network and cerebellum during reciprocity. ConclusionsThese findings suggest that closeness calibrates the striatal SRS link to regional activity and network-level responses during social exchange, while depression alters how striatal SRS relates to regional activity, potentially disrupting how individuals interpret and respond to close others.

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α-tACS Modulates Reward-Dependent Pupil Responses and Corticostriatal Connectivity

IntroductionNoninvasive brain stimulation can help clarify the neural basis of reward processing and potentially inform treatments for disorders involving reward dysfunction. However, widely used methods such as transcranial magnetic and electrical stimulation cannot directly stimulate deep-brain regions like the striatum. Here, we tested whether stimulating the ventrolateral prefrontal cortex (VLPFC)--a cortical region strongly connected to the striatum-- could indirectly influence reward-related neural and physiological responses. MethodsIn a within-subjects design, participants performed a card-guessing task involving monetary rewards for correct guesses and punishments for incorrect guesses. During the task, participants underwent functional magnetic resonance imaging (fMRI) and pupillometry while receiving concurrent 10 Hz transcranial alternating current stimulation (-tACS). Stimulation targeted either the VLPFC or a control region (temporoparietal junction). We measured pupil dilation, brain activation (BOLD signal), and functional connectivity between the ventral striatum and dorsal anterior cingulate cortex (VS-dACC). ResultsVLPFC stimulation increased pupil size during reward and punishment outcomes, indicating greater physiological arousal. At the neural level, -tACS enhanced VLPFC activation during reward and suppressed its responses during punishment. Stimulation also changed VS- dACC connectivity in a context-dependent manner. Importantly, stimulation-driven increases in pupil size during reward correlated positively with stimulation-induced changes in VS-dACC connectivity. Exploratory moderated mediation analyses suggested that stimulation influenced the degree to which striatal responses mediated the relationship between task outcomes and pupil size changes. ConclusionsTargeting VLPFC with -tACS modulates local cortical activity and corticostriatal networks during reward processing, providing a promising noninvasive approach to influence reward circuitry. HighlightsO_LI-tACS over VLPFC increases pupil responses to reward and punishment. C_LIO_LIStimulation alters reward-related VLPFC activity without enhancing striatal BOLD. C_LIO_LI-tACS modulates ventral striatum-dACC connectivity in a task-dependent manner. C_LIO_LIConnectivity changes predict pupil dilation, linking brain and autonomic responses. C_LI

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Neural and Behavioral Responses to Social Norm Violations Across Trust and Fairness Contexts

Trust and fairness sustain cooperation, but social neuroscience has largely studied violations of these social norms in isolation. We asked whether neural sensitivity to betrayal carries forward into the evaluation of unfairness in a separate social exchange. In 132 adults who completed fMRI during the Trust Game and Ultimatum Game, betrayal and unfairness both recruited overlapping voxels within left anterior insula. Yet, individual differences in regional activation were uncorrelated across tasks, arguing against a simple shared-response account. Instead, cross-task structure emerged in connectivity: stronger anterior insula responses to social versus nonsocial betrayal predicted weaker anterior insula-ventromedial prefrontal coupling during social versus nonsocial fairness evaluation. These findings suggest that betrayal and unfairness are linked less by identical regional responses than by how salience signals engage valuation circuitry across contexts. By bridging two canonical social exchange tasks within the same individuals, this study reveals a network-level architecture for generalizing sensitivity to interpersonal norm violations.

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Precision Imaging for Intraindividual Investigation of the Reward Response

The reliance of fMRI research on between-person comparisons is limited by low test-retest reliability and inability to explain within-person processes. Intraindividual studies are needed to understand how changes in brain functioning relate to changes in behavior. Here, we present open data and analysis of a novel intensively sampled fMRI study, the Night Owls Scan Club. This precision imaging dataset includes 44 sessions acquired across four participants at a twice-weekly rate. In each session, participants completed multiple reward-related tasks, mood and alertness ratings, and a behavioral mood manipulation. We examined how the reward response reflects between-person or within-person variance. Test-retest-reliability of the reward response was very low and not explained by measurement error, suggesting little utility for between-person comparisons. At an intraindividual level, the mood induction showed small increases in the reward anticipation response. Additionally, mood and alertness explained notable intraindividual variance of the reward response, including as much as 31% for one participant. Overall, results suggest that BOLD activation to reward tasks - and likely other fMRI tasks - is more appropriate for within-person study than between-person study, highlighting a need for intensive longitudinal neuroimaging designs.

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Older Adults Show Altered Network Connectivity during Fairness Decisions with Similar and Dissimilar Partners

Fairness-related decisions depend on both offer value and partner identity, yet how aging reshapes the network-level connectivity supporting these decisions across social contexts remains unknown. Younger (18-35) and older (65-80) adults underwent fMRI while responding to offers in an ultimatum game from ostensible partners similar or dissimilar in age. We modeled trial-by-trial choices by offer size, age group, and partner similarity, and examined whole-brain activation and task-dependent connectivity of the default mode (DMN) and executive control (ECN) networks. Participants accepted fairer offers more often, but behavioral sensitivity did not differ reliably by age group or partner similarity. Whole-brain activation analyses revealed no significant age-by-partner-similarity effects. Connectivity analyses, however, revealed opposing age-related patterns. Younger adults showed stronger fairness-modulated DMN-anterior cingulate connectivity for similar than for dissimilar partners, whereas older adults showed the reverse. Age also moderated the relationship between individual sensitivity to fairness norm violations and ECN-medial prefrontal connectivity: this association was negative in younger adults and positive in older adults. These findings suggest that decisions regarding fairness in younger and older adults may be supported by different patterns of large-scale network connectivity.

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The Cerebellum and Striatum in Reward Processing: Caring About Being Right vs. Caring About Reward

Emerging evidence indicates the cerebellum contributes to cognitive functions including social reward processing, yet its specific role relative to established reward regions like the ventral striatum remains undefined. We hypothesized the cerebellum would respond equivalently to both positive and negative social rewards. This prediction is grounded in classical findings that the cerebellum operates via supervised learning mechanisms that rely on error signals rather than traditional reward-based reinforcement. Using fMRI, we examined adolescents and young adults during a social prediction task where participants forecasted others opinions of them and received accuracy feedback. Findings reveal that both the ventral striatum and a subregion of the posterior cerebellum (Crus I and II) were sensitive to social rewards. However, unlike the ventral striatum, the cerebellum exhibited a more uniform response to feedback, treating correct predictions about being liked and disliked in a similar manner. No age-related differences were observed. These findings suggest the cerebellum processes social rewards distinctly from the ventral striatum, likely reflecting its computational emphasis on prediction errors rather than reward valence. This functional distinction advances our understanding of cerebellar contributions to social cognition and learning mechanisms.

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Trait reward sensitivity and behavioral motivation shape connectivity between the default mode network and the striatum during reward anticipation

Individuals vary substantially in their responses to rewarding events and their motivation to pursue rewards. While the ventral striatum (VS) plays a central role in reward anticipation, its functional connectivity with the default mode network (DMN)--critical for self-referential processing and value integration--potentially represents a key mechanism through which trait differences manifest in reward-related behavior. Here, we examine how trait reward sensitivity and state-level behavioral motivation relate to connectivity between the DMN and VS during reward anticipation. Forty-six participants completed the Monetary Incentive Delay task while undergoing fMRI, with trial types reflecting varying levels of reward and loss salience. Behavioral motivation, indexed by reaction time modulation across high-stakes and low-stakes trials, and self-report measures of anticipatory pleasure and reward sensitivity were assessed. Reward sensitivity interacted with anticipatory pleasure to predict behavioral motivation, such that individuals with higher anticipatory pleasure showed weaker behavioral motivation when reward sensitivity was greater, while those with lower anticipatory pleasure showed stonger behavioral motivation when reward sensitivity was greater. Critically, during high-stakes trials, reward sensitivity was associated with stronger DMN-VS connectivity in highly motivated individuals and weaker connectivity in less motivated participants. This moderation effect was consistent across gain and loss contexts, though with distinct directionality patterns. These findings provide novel insights into the neural correlates of individual differences in reward processing, demonstrating that trait reward sensitivity, anticipatory pleasure, and behavioral motivation are associated with distinct patterns of DMN-VS interactions during reward anticipation. These findings highlight the importance of considering motivational context when investigating reward-related neural mechanisms.

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Differential representations for affective and informative components of reward in the striatum and hippocampus

Receipt of a reward is composed of affective and informative components, which are often intertwined in most reward-processing and decision-making tasks. Our previous work allowed us to identify regions that were more strongly engaged for the affective and informative components of reward upon receipt (Smith et al., 2016) and showed that the ventral striatum responds to both affective and informative components of reward processing. However, the limited spatial resolution and coarse analytical approaches made it hard to understand how these different components of reward were represented in the brain, wherein similar engagement may not necessitate similar representations. In our current study, we used high-resolution functional magnetic resonance imaging (voxel size: 1.75 mm3) and representational similarity analysis to investigate the representation of affective and informative components of reward receipt in the striatum and the hippocampus, another region that is sensitive to reward information. We found a differential representation of affective and informative components of reward receipt in the striatum and the hippocampus, with no difference in representation between the two structures. However, in the dorsal striatum, we found that representations were stronger for affective rather than the informative components of reward receipt. Finally, we observed that the ventral striatum was sensitive to the predictiveness of information, such that across-run pattern similarity in the ventral striatum increased with the predictiveness of information. In sum, our results provide evidence of how affective and informative components of rewards are represented in the striatum and the hippocampus, potentially indicating a differential coding schema for the dorsal and the ventral striatum.

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

Explore-exploit research faces challenges in generalizability due to a limited theoretical basis for exploration and exploitation. Neuroimaging can help identify whether explore-exploit decisions involve an opponent processing system to address this issue. Thus, we conducted a coordinate-based meta-analysis (N=23 studies) finding activation in the dorsal lateral prefrontal cortex, anterior insula, and anterior cingulate cortex during exploration versus exploitation, which provides some evidence for opponent processing. However, the conjunction of explore-exploit decisions was associated with activation in the dorsal anterior cingulate cortex and dorsal medial prefrontal cortex, suggesting that these brain regions do not engage in opponent processing. Furthermore, exploratory analyses revealed heterogeneity in brain responses between task types during exploration and exploitation respectively. Coupled with results suggesting that activation during exploration and exploitation decisions is generally more similar than it is different suggests that there remain significant challenges in characterizing explore-exploit decision making. Nonetheless, dorsal lateral prefrontal cortex, anterior insula, and dorsal anterior cingulate cortex activation differentiate explore and exploit decisions and identifying these responses can aid in targeted interventions aimed at manipulating these decisions. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=161 SRC="FIGDIR/small/563317v4_ufig1.gif" ALT="Figure 1"> View larger version (51K): org.highwire.dtl.DTLVardef@172abbeorg.highwire.dtl.DTLVardef@16948b6org.highwire.dtl.DTLVardef@124d4a3org.highwire.dtl.DTLVardef@1042f75_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical AbstractC_FLOATNO We conducted a coordinate-based meta-analysis (N=23 studies) where we found activation in the dorsal lateral prefrontal cortex, anterior insula, and the anterior cingulate cortex during exploration versus exploitation. However, the conjunction of explore-exploit decisions was associated with activation in the dorsal medial prefrontal cortex, and the insula, suggesting that these brain regions do not engage in opponent processing. Nonetheless, activation that differentiates explore and exploit decisions and can help in targeted interventions aimed at manipulating these decisions. C_FIG

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Social Context and Reward Sensitivity Enhance Corticostriatal Function during Experiences of Shared Rewards

Although prior research has demonstrated enhanced striatal response when sharing rewards with close social connections, less is known about how individual differences affect ventral striatal (VS) activation and connectivity when experiencing rewards within social contexts. Given that self-reported reward sensitivity and level of substance use have been associated with differences in VS activation, we set out to investigate whether these factors would be independently associated with enhancements to neural reward responses within social contexts. In this pre-registered study, participants (N=45) underwent fMRI while playing a card guessing game in which correct or incorrect guesses resulted in monetary gains and losses that were shared evenly with either a close friend, stranger (confederate), or non-human partner. Consistent with our prior work, we found increased VS activation when sharing rewards with a socially close peer as opposed to an out-of-network stranger. As self-reported reward sensitivity increased, the difference in VS response to rewards shared with friends and strangers decreased. We also found enhanced connectivity between the VS and temporoparietal junction when sharing rewards with close friends as opposed to strangers. Finally, exploratory analyses revealed that as reward sensitivity and sub-clinical substance use increase, the difference in VS connectivity with the right fusiform face area increases as a function of social context. These findings demonstrate that responsivity to the context of close friends may be tied to individual reward sensitivity or sub-clinical substance use habits; together these factors may inform predictions of risk for future mental health disorders.

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

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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Substance use is related to differential activation and connectivity for social relative to monetary rewards

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.

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Tensorial Independent Component Analysis Reveals Social and Reward Networks Associated with Major Depressive Disorder

Major depressive disorder (MDD) has been associated with changes in functional brain connectivity. Yet, typical analyses of functional connectivity, such as spatial ICA for resting-state data, often ignore sources of between-subject variability, which may be crucial for identifying functional connectivity patterns associated with MDD. Typically, methods like spatial ICA will identify a single component to represent a network like the default mode network (DMN), even if groups within the data show differential DMN coactivation. To address this gap, this project applies a tensorial extension of ICA (tensorial ICA)--which explicitly incorporates between-subject variability--to identify functionally connected networks using fMRI data from the Human Connectome Project (HCP). Data from the HCP included individuals with a diagnosis of MDD, a family history of MDD, and healthy controls performing a gambling and social cognition task. Based on evidence associating MDD with blunted neural activation to rewards and social stimuli, we predicted that tensorial ICA would identify networks associated with reduced spatio-temporal coherence and blunted social and reward-based network activity in MDD. Across both tasks, tensorial ICA identified three networks showing decreased coherence in MDD. All three networks included ventromedial prefrontal cortex (vmPFC), striatum, and cerebellum and showed different activation across the conditions of their respective tasks. However, MDD was only associated with differences in task-based activation in one network from the social task. Additionally, these results suggest that tensorial ICA could be a valuable tool for understanding clinical differences in relation to network activation and connectivity.

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Age-Related Differences in Ventral Striatal and Default Mode Network Function During Reciprocated Trust

Social relationships change across the lifespan as social networks narrow and motivational priorities shift to the present. Interestingly, aging is also associated with changes in executive function, including decision-making abilities, but it remains unclear how age-related changes in both domains interact to impact financial decisions involving other people. To study this problem, we recruited 50 human participants (Nyounger = 26, ages 18-34; Nolder = 24, ages 63-80) to play an economic trust game as the investor with three partners (friend, stranger, and computer) who played the role of investee. Investors underwent functional magnetic resonance imaging (fMRI) during the trust game while investees were seated outside of the scanner. Building on our previous work with younger adults showing both enhanced striatal responses and altered default-mode network (DMN) connectivity as a function of social closeness during reciprocated trust, we predicted that these relations would exhibit age-related differences. We found that striatal responses to reciprocated trust from friends relative to strangers and computers were blunted in older adults relative to younger adults, thus supporting our primary pre-registered hypothesis regarding social closeness. We also found that older adults exhibited enhanced DMN connectivity with the temporoparietal junction (TPJ) during reciprocated trust from friends compared to computers while younger adults exhibited the opposite pattern. Taken together, these results advance our understanding of age-related differences in sensitivity to social closeness in the context of trusting others.

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Reward Enhances Connectivity between the Ventral Striatum and the Default Mode Network

The default mode network (DMN) has been theorized to participate in a range of social, cognitive, and affective functions. Yet, previous accounts do not consider how the DMN contributes to other brain regions depending on psychological context, thus rendering our understanding of DMN function incomplete. We addressed this gap by applying a novel network-based psychophysiological interaction (nPPI) analysis to the reward task within the Human Connectome Project. We first focused on the task-evoked responses of the DMN and other networks involving the prefrontal cortex, including the executive control network (salience network) and the left and right frontoparietal networks. Consistent with a host of prior studies, the DMN exhibited a relative decrease in activation during the task, while the other networks exhibited a relative increase during the task. Next, we used nPPI analyses to assess whether these networks exhibit task-dependent changes in connectivity with other brain regions. Strikingly, we found that the experience of reward enhances task-dependent connectivity between the DMN and the ventral striatum, an effect that was specific to the DMN. Surprisingly, the strength of DMN-VS connectivity was correlated with personality characteristics relating to openness. Taken together, these results advance models of DMN by demonstrating how it contributes to other brain systems during task performance and how those contributions relate to individual differences.

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Distinct Alterations in Cerebellar Connectivity with Substantia Nigra and Ventral Tegmental Area in Parkinsons Disease

In Parkinsons disease (PD), neurodegeneration of dopaminergic neurons occurs in the midbrain, specifically targeting the substantia nigra (SN), while leaving the ventral tegmental area (VTA) relatively spared in early phases of the disease. Although the SN and VTA are known to be functionally dissociable in healthy adults, it remains unclear how this dissociation is altered in PD. To examine this issue, we performed a whole-brain analysis to compare functional connectivity in PD to healthy adults using resting-state functional magnetic resonance imaging (rs-fMRI) data compiled from three independent datasets. Our analysis showed that across the sample, the SN had greater connectivity with the precuneus, anterior cingulate gyrus, and areas of the occipital cortex, partially replicating our previous work in healthy young adults. Notably, we also found that, in PD, VTA-right cerebellum connectivity was higher than SN-right cerebellum connectivity, whereas the opposite trend occurred in healthy controls. This double dissociation may reflect a compensatory role of the cerebellum in PD and could provide a potential target for future study and treatment.

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