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.

An fMRI dataset of social and nonsocial reward processing in young adults.

Trait reward sensitivity, risk for developing substance use, and mood disorders have each been linked with altered striatal responses to reward. Moreover, striatal response to reward is sensitive to social context, such as the presence of a peer, and drugs are often sought out and consumed in social contexts or as a result of social experiences. Thus, mood disorder symptoms, striatal responses to social context and social reward may play a role in substance use. To investigate this possibility, this dataset was collected as part of a National Institute on Drug Abuse (NIDA) grant titled "Aberrant Reward Sensitivity: Mechanisms Underlying Substance Use" (R03-DA046733). The overarching goal was to characterize the associations between neural responses to social and nonsocial rewards, trait reward sensitivity, substance use, and mood disorder symptoms. After obtaining questionnaire data quantifying reward sensitivity, substance use, and other psychosocial characteristics, young adults (N=59; 14 male, 45 female; mean age: 20.89 years ± 1.75 years) completed four fMRI tasks testing different features of social and reward processing. These included: 1) a strategic reward-based decision-making task with Ultimatum and Dictator Game conditions; 2) a task where participants shared rewards or losses with peers, strangers, or non-human partners; 3) a task in which participants received well-matched social and monetary rewards and punishment; and 4) a monetary incentive delay (MID) task in which participants tried to obtain or avoid rewards and losses of different magnitude. This dataset includes sociodemographic questionnaire data, anatomical, task-based fMRI, and corresponding behavioral task-based data. We outline several opportunities for extension and reuse, including exploration of individual differences, cross-task comparisons, and representational similarity analyses.

An fMRI Dataset on Social Reward Processing and Decision Making in Younger and Older Adults.

Behavioural and neuroimaging research has shown that older adults are less sensitive to financial losses compared to younger adults. Yet relatively less is known about age-related differences in social decisions and social reward processing. As part of a pilot study, we collected behavioural and functional magnetic resonance imaging (fMRI) data from 50 participants (Younger: N = 26, ages 18-34 years; Older: N = 24, ages 63-80 years) who completed three tasks in the scanner: an economic trust game as the investor with three partners (computer, stranger, friend) as the investee; a card-guessing task with monetary gains and losses shared with three partners (computer, stranger, friend); and an ultimatum game as responder to three anonymous proposers (computer, age-similar adults, age-dissimilar adults). We also collected B0 field maps and high-resolution structural images (T1-weighted and T2-weighted images). These data could be reused to answer questions about moment-to-moment variability in fMRI signal, representational similarity between tasks, and brain structure.

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.

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 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.

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.

Motivation as a Lens for Understanding Information-seeking Behaviors.

Most prior research characterizes information-seeking behaviors as serving utilitarian purposes, such as whether the obtained information can help solve practical problems. However, information-seeking behaviors are sensitive to different contexts (i.e., threat vs. curiosity), despite having equivalent utility. Furthermore, these search behaviors can be modulated by individuals' life history and personality traits. Yet the emphasis on utilitarian utility has precluded the development of a unified model, which explains when and how individuals actively seek information. To account for this variability and flexibility, we propose a unified information-seeking framework that examines information-seeking through the lens of motivation. This unified model accounts for integration across individuals' internal goal states and the salient features of the environment to influence information-seeking behavior. We propose that information-seeking is determined by motivation for information, invigorated either by instrumental utility or hedonic utility, wherein one's personal or environmental context moderates this relationship. Furthermore, we speculate that the final common denominator in guiding information-seeking is the engagement of different neuromodulatory circuits centered on dopaminergic and noradrenergic tone. Our framework provides a unified framework for information-seeking behaviors and generates several testable predictions for future studies.

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.

When thinking you are better leads to feeling worse: Self-other asymmetries in pro-social behavior and increased anxiety during Covid-19.

Self-serving biases (e.g., beliefs that one tends to perform better than peers) are generally associated with positive psychological outcomes like increased self-esteem and resilience. However, this tendency may be problematic in the context of collective action problems, wherein individuals are reliant on others' pro-social behaviors to achieve larger goals. We examined this question in the context of the Covid-19 pandemic, and recruited participants for an online study (n = 1023) from a university community in Spring 2020. We found evidence for self-peer asymmetries in Covid-related knowledge and restriction behavior, such that participants reported that they knew more about Covid-related symptoms, were doing more to stop the spread of the disease, and were more pro-socially motivated in doing so than peers. Actual peer reports indicated that these were overestimations. This self-enhancement comes with a cost: the perceived self-peer restriction behavior asymmetry had an indirect effect on the positive relationships both from Covid-specific worry and from perceived stress to general anxiety symptom intensity during the early lockdown period. People tended to have more severe symptoms of anxiety when they were more worried about Covid-19 and when they reported greater perceived stress, especially when they underestimated others' contributions to public health action relative to their own. This suggests that lack of trust in others' pro-sociality may be personally maladaptive for mental health.

Characterizing heterogeneity in early adolescent reward networks and individualized associations with behavioral and clinical outcomes.

Associations between connectivity networks and behavioral outcomes such as depression are typically examined by comparing average networks between known groups. However, neural heterogeneity within groups may limit the ability to make inferences at the individual level as qualitatively distinct processes across individuals may be obscured in group averages. This study characterizes the heterogeneity of effective connectivity reward networks among 103 early adolescents and examines associations between individualized features and multiple behavioral and clinical outcomes. To characterize network heterogeneity, we used extended unified structural equation modeling to identify effective connectivity networks for each individual and an aggregate network. We found that an aggregate reward network was a poor representation of individuals, with most individual-level networks sharing less than 50% of the group-level network paths. We then used Group Iterative Multiple Model Estimation to identify a group-level network, subgroups of individuals with similar networks, and individual-level networks. We identified three subgroups that appear to reflect differences in network maturity, but this solution had modest validity. Finally, we found numerous associations between individual-specific connectivity features and behavioral reward functioning and risk for substance use disorders. We suggest that accounting for heterogeneity is necessary to use connectivity networks for inferences precise to the individual.

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 independent components analysis (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 functional MRI 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 spatiotemporal 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, 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.

Stress, trauma, and perception of eating behavior changes during the first weeks of the COVID-19 outbreak.

OBJECTIVE: The COVID-19 pandemic is one of the largest collective stressors in recent history. Consistent with prior research, this stress has led to impactful eating behavior change. While prior life traumas also impact eating behavior, it is unclear whether the current stress experienced during COVID-19, and prior life traumas (overall, socially relevant, and nonsocially relevant), interact to influence eating behavior changes. Moreover, it is unclear whether current stress and prior traumas impact how eating behavior changes are perceived (i.e., in magnitude, valence, or both) by the individuals experiencing the changes. Therefore, this study sought to examine both the relationship between current stress and perception of eating behavior changes, as well as the moderating impact of prior life traumas on this relationship. METHODS: Between March and April 2020, participants completed a subjective, self-report online assessment of current stress, prior life traumas, pandemic-related changes in eating behaviors, and the perceived impact of eating behavior changes. RESULTS: Higher current stress was associated with larger, more negative perceptions of eating behavior changes. This relationship was moderated by prior life traumas. Specifically, the association between current stress and perceived negative impact of eating behavior change was potentiated among those with more prior socially relevant (but not nonsocially relevant) traumas. DISCUSSION: These results suggest eating behavior changes occurred early in the pandemic and were uniquely impacted by the cumulative effect of present stress and socially relevant prior life traumas. PUBLIC SIGNIFICANCE: Changes in eating behaviors and pathology have been prevalent during COVID-19. We examined how stress and prior life traumas interacted during the first weeks of COVID-19 to influence perceptions of eating behavior change. As altered perception of eating behaviors is a notable feature of eating pathology, these results will help inform development of intervention targets for those at risk for developing disordered eating during future- and post-pandemic recovery.

Machine-learning as a validated tool to characterize individual differences in free recall of naturalistic events.

The use of naturalistic stimuli, such as narrative movies, is gaining popularity in many fields, characterizing memory, affect, and decision-making. Narrative recall paradigms are often used to capture the complexity and richness of memory for naturalistic events. However, scoring narrative recalls is time-consuming and prone to human biases. Here, we show the validity and reliability of using a natural language processing tool, the Universal Sentence Encoder (USE), to automatically score narrative recalls. We compared the reliability in scoring made between two independent raters (i.e., hand scored) and between our automated algorithm and individual raters (i.e., automated) on trial-unique video clips of magic tricks. Study 1 showed that our automated segmentation approaches yielded high reliability and reflected measures yielded by hand scoring. Study 1 further showed that the results using USE outperformed another popular natural language processing tool, GloVe. In Study 2, we tested whether our automated approach remained valid when testing individuals varying on clinically relevant dimensions that influence episodic memory, age, and anxiety. We found that our automated approach was equally reliable across both age groups and anxiety groups, which shows the efficacy of our approach to assess narrative recall in large-scale individual difference analysis. In sum, these findings suggested that machine learning approach implementing USE is a promising tool for scoring large-scale narrative recalls and perform individual difference analysis for research using naturalistic stimuli.

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.

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.

Distinct alterations in cerebellar connectivity with substantia nigra and ventral tegmental area in Parkinson's disease.

In Parkinson's 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.

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.

Decision uncertainty during hypothesis testing enhances memory accuracy for incidental information.

Humans actively seek information to reduce uncertainty, providing insight on how our decisions causally affect the world. While we know that episodic memories can help support future goal-oriented behaviors, little is known about how hypothesis testing during exploration influences episodic memory. To investigate this question, we designed a hypothesis testing paradigm, in which participants figured out rules to unlock treasure chests. Using this paradigm, we characterized how hypothesis testing during exploration influenced memory for the contents of the treasure chests. We found that there was an inverted U-shaped relationship between decision uncertainty and memory, such that memory was best when decision uncertainty was moderate. An exploratory analysis also showed that surprising outcomes lead to lower memory confidence independent of accuracy. These findings support a model in which moderate decision uncertainty during hypothesis testing enhances incidental information encoding.

Decision neuroscience and neuroeconomics: Recent progress and ongoing challenges.

In the past decade, decision neuroscience and neuroeconomics have developed many new insights in the study of decision making. This review provides an overarching update on how the field has advanced in this time period. Although our initial review a decade ago outlined several theoretical, conceptual, methodological, empirical, and practical challenges, there has only been limited progress in resolving these challenges. We summarize significant trends in decision neuroscience through the lens of the challenges outlined for the field and review examples where the field has had significant, direct, and applicable impacts across economics and psychology. First, we review progress on topics including reward learning, explore-exploit decisions, risk and ambiguity, intertemporal choice, and valuation. Next, we assess the impacts of emotion, social rewards, and social context on decision making. Then, we follow up with how individual differences impact choices and new exciting developments in the prediction and neuroforecasting of future decisions. Finally, we consider how trends in decision-neuroscience research reflect progress toward resolving past challenges, discuss new and exciting applications of recent research, and identify new challenges for the field. This article is categorized under: Psychology > Reasoning and Decision Making Psychology > Emotion and Motivation.

Family history of depression is associated with alterations in task-dependent connectivity between the cerebellum and ventromedial prefrontal cortex.

BACKGROUND: A family history of major depressive disorder (MDD) increases the likelihood of a future depressive episode, which itself poses a significant risk for disruptions in reward processing and social cognition. However, it is unclear whether a family history of MDD is associated with alterations in the neural circuitry underlying reward processing and social cognition. METHODS: We subdivided 279 participants from the Human Connectome Project into three groups: 71 with a lifetime history of MDD, 103 with a family history (FH) of MDD, and 105 healthy controls (HCs). We then evaluated task-based functional magnetic resonance imaging data on a social cognition and a reward processing task and found a region of the ventromedial prefrontal cortex (vmPFC) that responded to both tasks, independent of the group. To investigate whether the vmPFC shows alterations in functional connectivity between groups, we conducted psychophysiological interaction analyses using the vmPFC as a seed region. RESULTS: We found that FH (relative to HC) was associated with increased sadness scores, and MDD (relative to both FH and HC) was associated with increased sadness and MDD symptoms. Additionally, the FH group had increased vmPFC functional connectivity within the nucleus accumbens, left dorsolateral PFC, and subregions of the cerebellum relative to HC during the social cognition task. CONCLUSIONS: These findings suggest that aberrant neural mechanisms among those with a familial risk of MDD may underlie vulnerability to altered social cognition.