Impact of social reward on stress circuit function and regulation: Path differences between value affirmation and emotional support.

Background: As two typical types of social rewards, both value affirmation and emotional support could alleviate acute stress response, but it is not clear whether they can impact stress circuit function and regulation through different neural pathways. Method: Sixty-two participants were randomly assigned to the value affirmation, emotional support, and non-reward conditions, then administered an adapted version of the ScanSTRESS paradigm. Participants' subjective reports of uncontrollability and social evaluative threat were measured to explore the mitigation of stress by social rewards at the behavioral level. Meanwhile, their acute salivary cortisol response to stress was compared among different social reward conditions. Furthermore, we computed linear contrasts for performance (vs relaxation) and reward (vs non-reward) and used psychophysiological interaction (PPI) analysis to explore the impact of social reward on stress circuit function and regulation. Results: Both value affirmation and emotional support conditions reduced subjective reports of uncontrollability and social evaluation threat, but not cortisol response to stress. Furthermore, value affirmation reduced uncontrollability by enhancing putamen activation, whereas emotional support reduced social evaluation threat by enhancing putamen activation. More importantly, during stress, value affirmation enhanced the functional connectivity of the putamen-hippocampus and putamen-angular gyrus (AG), whereas emotional support enhanced the functional connectivity of the putamen-ventrolateral prefrontal cortex (vlPFC) and putamen-temporal pole mid, compared to the non-reward condition. Conclusion: Value affirmation and emotional support alleviated acute stress response in different neural pathways. These findings suggested a precise categorization of social reward in intervention of a range of adverse psychological and physiological responses caused by stress.

Blunted reward-related activation to food scenes distinguishes individuals with alcohol use disorder in a pilot case-control fMRI pilot study.

BACKGROUND: Alcohol use disorder (AUD) is thought to bias the neurocircuitry underlying reward processing and motivation to preferentially attend to conditioned alcohol cues over natural rewards. The present case-control pilot study evaluated this hypothesis using novel natural reward paradigms. METHODS: Twenty-eight participants (AUD, n = 14, light drinkers, n = 14) were recruited-AUD participants reported 44.0% heavy drinking days (%HDD) and 4.67 drinks/day over the preceding 90 days. Functional magnetic resonance imaging (fMRI) data were acquired during the administration of three separate picture-viewing paradigms of alcohol cues, food scenes, and social reward, respectively. Independent samples t-tests were performed to compare groups' fMRI data and exploratory correlation analyses were performed to examine associations with clinical characteristics of AUD. RESULTS: Food scenes elicited abnormally low reward-related activation, within the superior frontal gyrus and caudate bilaterally, among AUD participants. Lower activation to food scenes within the superior frontal gyrus was, in turn, associated with higher levels of past-month %HDD among AUD participants, specifically, along with craving and alcohol dependence severity when examined across the full sample. Contrasting reward types (e.g., alcohol cues vs. food scenes) did not reveal "preferential" activation to differentiate groups. CONCLUSIONS: Heavy drinking appears associated with reduced responsivity to natural rewards, specifically food rather than social cues. Neural mechanisms underlying the high prevalence of malnutrition among individuals with AUD may involve some combination of blunted approach-related affect and reduced craving-related motivation to eat when food is present, resulting in limited engagement of cortico-striato-thalamic motor circuitry supporting food acquisition. However, given the preliminary nature of this pilot study, such formulations remain tentative until larger follow-up studies can be conducted. From a potential translational standpoint, the ability of promising therapeutics to demonstrate increased responsivity to natural rewards, specifically nutritive reward may serve as a valuable complementary efficacy indicator for future clinical neuroimaging trials in AUD.

How adolescents learn to build social bonds: A developmental computational account of social explore-exploit decision-making.

Building social bonds is a critical task of adolescence that affords opportunities for learning, identity formation, and social support. Failing to develop close relationships in adolescence hinders adult interpersonal functioning and contributes to problems such as loneliness and depression. During adolescence, increased reward sensitivity and greater social flexibility both contribute to healthy social development, yet we lack a clear theory of how these processes interact to support social functioning. Here, we propose synthesizing these two literatures using a computational reinforcement learning framework that recasts how adolescents pursue and learn from social rewards as a social explore-exploit problem. To become socially skilled, adolescents must balance both their efforts to form individual bonds within specific groups and manage memberships across multiple groups to maximize access to social resources. We draw on insights from sociological studies on social capital in collective networks and neurocognitive research on foraging and cooperation to describe the social explore-exploit dilemma faced by adolescents navigating a modern world with increasing access to diverse resources and group memberships. Our account provides important new directions for examining the dynamics of adolescent behavior in social groups and understanding how social value computations can support positive relationships into adulthood.

The enhancing effect of social reward on inhibitory control in smokers: Evidence from behaviour and ERP studies.

OBJECTIVE: Prior research has revealed impaired inhibitory control as a pivotal factor contributing to smokers' struggle to control smoking impulses. However, few studies focus on enhancing smokers' inhibitory control. This study investigates the potential of social rewards to bolster inhibitory control among smokers and elucidates the underlying mechanisms. METHODS: In Experiment 1, a reward-based Go/Nogo paradigm assessed error rates and reaction times for 30 smokers exposed to social reward and neutral feedback in distinct contexts (smoking-related and neutral). Experiment 2 used a modified paradigm, incorporating cognitive load manipulation, to investigate error rates, reaction times, N2, and P3 ERPs among 32 smokers facing social reward and neutral feedback under different cognitive loads (high and low). RESULTS: Smokers exhibit lower Nogo error rates with social reward feedback; higher error rates occur with smoking cues and high cognitive load; increased N2, P3 amplitudes under social reward versus neutral feedback; low cognitive load enhances P3 amplitude under social reward. CONCLUSION: Social reward improves smokers' inhibitory control, but this effect weakens with exposure to smoking cues; higher cognitive load further diminishes the enhancement of smokers' inhibitory control by social reward under smoking cues.

Linking social reward responsiveness and affective responses to the social environment: An ecological momentary assessment study.

Social support is a key predictor of well-being, but not everyone experiences mental health benefits from receiving it. However, given that a growing number of interventions are based on social support, it is crucial to identify the features that make individuals more likely to benefit from social ties. Emerging evidence suggests that neural responses to positive social feedback (i.e., social reward) might relate to individual differences in social functioning, but potential mechanisms linking these neural responses to psychological outcomes are yet unclear. This study examined whether neural correlates of social reward processing, indexed by the reward positivity (RewP), relate to individuals' affective experience following self-reported real-world positive social support events. To this aim, 193 university students (71% females) underwent an EEG assessment during the Island Getaway task and completed a 10-day ecological momentary assessment where participants reported their positive and negative affects (PA, NA) nine times a day and the count of daily positive and negative events. Experiencing a higher number of social support positive events was associated with higher PA. The RewP moderated this association, such that individuals with greater neural response to social feedback at baseline had a stronger positive association between social support positive events count and PA. Individual differences in the RewP to social feedback might be one indicator of the likelihood of experiencing positive affect when receiving social support.

RNA-sequencing reveals a shared neurotranscriptomic profile in the medial preoptic area of highly social songbirds and rats.

Rough-and-tumble play in juvenile rats and song in flocks of adult songbirds outside a breeding context (gregarious song) are two distinct forms of non-sexual social behavior. Both are believed to play roles in the development of sociomotor skills needed for later life-history events, including reproduction, providing opportunities for low-stakes practice. Additionally, both behaviors are thought to be intrinsically rewarded and are associated with a positive affective state. Given the functional similarities of these behaviors, this study used RNA-sequencing to identify commonalities in their underlying neurochemical systems within the medial preoptic area. This brain region is implicated in multiple social behaviors, including song and play, and is highly conserved across vertebrates. DESeq2 and rank-rank hypergeometric overlap analyses identified a shared neurotranscriptomic profile in adult European starlings singing high rates of gregarious song and juvenile rats playing at high rates. Transcript levels for several glutamatergic receptor genes, such as GRIN1, GRIN2A, and GRIA1, were consistently upregulated in highly gregarious (i.e., playful/high singing) animals. This study is the first to directly investigate shared neuromodulators of positive, non-sexual social behaviors across songbirds and mammals. It provides insight into a conserved brain region that may regulate similar behaviors across vertebrates.

Aberrant social reward dynamics in individuals with melancholic major depressive disorder: An ERP study.

BACKGROUND: Compared to monetary rewards, depressive symptoms are specifically associated with abnormal social reward processing. In addition, individuals with melancholic depression may exhibit more significant reward-related impairments. However, there is still limited understanding of the specific alterations in social reward processing in individuals with melancholic depression. METHODS: Forty patients with melancholic major depressive disorder (MDD), forty patients with non-melancholic MDD, and fifty healthy controls participated in the social incentive delay (SID) tasks with event-related potential (ERP) recording. We measured one anticipatory ERP(cue-N2) and two consummatory ERPs (FRN, fb-P3). Furthermore, we examined correlation between FRN and consummatory anhedonia. RESULTS: Melancholic MDD patients showed less anticipation of social rewards (cue-N2). Concurrently, melancholic individuals demonstrated diminished reception of social rewards, as evidenced by reduced amplitudes of FRN. Notably, the group x condition interaction effect on FRN was significant (F (2, 127) = 4.15, p = 0.018, η2ρ = 0.061). Melancholic MDD patients had similar neural responses to both gain and neutral feedback (blunted reward positivity), whereas non-melancholic MDD patients (t (39) = 3.09, p = 0.004) and healthy participants (t (49) = 5.25, p < 0.001) had smaller FRN amplitudes when receiving gain feedback relative to neutral feedback. In addition, there was a significant correlation between FRN and consummatory anhedonia in MDD patients. CONCLUSIONS: Our findings indicated that individuals with melancholic MDD exhibit attenuated neural responses to both anticipated and consumed social rewards. This suggests that aberrant processing of social rewards could serve as a potential biomarker for melancholic MDD.

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 power modulates individuals' neural responses to monetary and social rewards.

Although previous research has shown that social power modulates individuals' sensitivity to rewards, it is currently unclear whether social power increases or decreases individuals' sensitivity to rewards. This study employed event-related potentials (ERPs) to investigate the effects of social power on individuals' neural responses to monetary and social rewards. Specifically, participants underwent an episodic priming task to manipulate social power (high-power vs. low-power) and then completed monetary and social delayed incentive tasks while their behavioral responses and electroencephalograms (EEG) were recorded. According to ERP analysis, during the anticipatory stage, low-power individuals exhibited a greater cue-P3 amplitude than high-power individuals in both monetary and social tasks. In the consummatory stage, though no impact of social power on the reward positivity (RewP) was found, low-power individuals showed a higher feedback-P3 (FB-P3) amplitude than high-power individuals, regardless of task types (the MID and SID tasks). In conclusion, these results provide evidence that social power might decrease one's sensitivity to monetary and social rewards in both the anticipatory and consummatory stages.

Novel rat model of gaming disorder: assessment of social reward and sex differences in behavior and c-Fos brain activity.

RATIONALE: In 2018, the International Classification of Diseases (ICD-11) classified Gaming Disorder (GD) as a mental disorder. GD mainly occurs among adolescents, who, after developing addiction, show psychopathological traits, such as social anxiety, depression, social isolation, and attention deficit. However, the different studies conducted in humans so far show several limitations, such as the lack of demographic heterogeneity and equal representation of age, differences in the type of game and in the follow-up period. Furthermore, at present, no animal models specific to GD are available. OBJECTIVES: To address the lack of an experimental model for GD, in the present work, we proposed a new GD rat model to investigate some peculiar tracts of the disorder. METHODS: Two-month-old Wistar Kyoto rats, both males and females, were subject to a five-week training with a new innovative touch-screen platform. After five weeks of training, rats were assessed for: (a) their attachment to the play under several conditions, (b) their hyperactivity during gaming, and (c) the maintenance of these conditions after a period of game pause and reward interruption. After sacrifice, using immunohistochemistry techniques, the immunoreactivity of c-Fos (a marker of neuronal activity) was analyzed to study different neural areas. RESULTS: After the training, the rats subjected to GD protocol developed GD-related traits (e.g., hyperactivity, loss control), and the behavioral phenotype was maintained consistently over time. These aspects were completely absent in the control groups. Lastly, the analysis of c-Fos immunoreactivity in prelimbic cortex (PrL), orbitofrontal cortex (OFC), nucleus Accumbens, amygdala and bed nucleus of stria terminalis (BNST) highlighted significant alterations in the GD groups compared to controls, suggesting modifications in neural activity related to the development of the GD phenotype. CONCLUSIONS: The proposal of a new GD rat model could represent an innovative tool to investigate, in both sexes, the behavioral and neurobiological features of this disorder, the possible role of external factors in the predisposition and susceptibility and the development of new pharmacological therapies.

Operant social self-administration in male CD1 mice.

RATIONALE AND OBJECTIVE: We recently introduced a model of operant social reward in which female CD1 mice lever press for access to affiliative social interaction with a cagemate peer mouse of the same sex and strain. Here we determined the generality of the operant social self-administration model to male CD1 mice who, under certain conditions, will lever press to attack a subordinate male mouse. METHODS: We trained male CD1 mice to lever press for food and social interaction with a same sex and strain cagemate peer under different fixed-ratio (FR) schedule response requirements (FR1 to FR6). We then tested their motivation to seek social interaction after 15 days of isolation in the presence of cues previously paired with social self-administration. We also determined the effect of housing conditions on operant social self-administration and seeking. Finally, we determined sex differences in operant social self-administration and seeking, and the effect of housing conditions on unconditioned affiliative and antagonistic (aggressive) social interactions in both sexes. RESULTS: Male CD1 mice lever pressed for access to a cagemate peer under different FR response requirements and seek social interaction after 15 isolation days; these effects were independent of housing conditions. There were no sex differences in operant social self-administration and seeking. Finally, group-housed CD1 male mice did not display unconditioned aggressive behavior toward a peer male CD1 mouse. CONCLUSIONS: Adult socially housed male CD1 mice can be used in studies on operant social reward without the potential confound of operant responding to engage in aggressive interactions.

Impaired social reward processing in individuals with Internet gaming disorder and its relationship with early face perception.

Previous research has found that individuals with Internet gaming disorder (IGD) show different patterns of social function impairments in game-related and real-life social contexts. Impaired social reward processing may be the underlying mechanism according to the Social Motivation Theory. Thus, in this study, event-related potentials were recorded from 24 individuals with IGD and 24 healthy gamers during a social judgement task. We focused on reward positivity (RewP) elicited by game-related and real-life social rewards, and N170 elicited by game avatar faces and real faces. These indicators were used to explore the neurocognitive mechanism of impaired social reward processing in individuals with IGD and its relationship with early face perception. Results showed that (1) the RewP elicited by real-life social reward was considerably reduced in individuals with IGD relative to healthy gamers. (2) The N170 elicited by game avatar faces in individuals with IGD was larger than that elicited by real faces. However, the N170 was not associated with RewP in either group. (3) The score for IGD severity was correlated with the RewP elicited by real-life social reward and the N170 elicited by game avatar face. In conclusion, the present study suggests that the impaired social reward processing in individuals with IGD is mainly manifested in a decreased neural sensitivity to real-life social reward. Meanwhile, the reduced RewP elicited by real-life social reward and the enhanced N170 elicited by game avatar face might serve as potential biomarkers for IGD.

Engagement of basal amygdala-nucleus accumbens glutamate neurons in the processing of rewarding or aversive social stimuli.

Basal amygdala (BA) neurons projecting to nucleus accumbens (NAc) core/shell are primarily glutamatergic and are integral to the circuitry of emotional processing. Several recent mouse studies have addressed whether neurons in this population(s) respond to reward, aversion or both emotional valences. The focus has been on processing of physical emotional stimuli, and here, we extend this to salient social stimuli. In male mice, an iterative study was conducted into engagement of BA-NAc neurons in response to estrous female (social reward, SR) and/or aggressive-dominant male (social aversion, SA). In BL/6J mice, SR and SA activated c-Fos expression in a high and similar number/density of BA-NAc neurons in the anteroposterior intermediate BA (int-BA), whereas activation was predominantly by SA in posterior (post-)BA. In Fos-TRAP2 mice, compared with SR-SR or SA-SA controls, exposure to successive presentation of SR-SA or SA-SR, followed by assessment of tdTomato reporter and/or c-Fos expression, demonstrated that many int-BA-NAc neurons were activated by only one of SR and SA; these SR/SA monovalent neurons were similar in number and present in both magnocellular and parvocellular int-BA subregions. In freely moving BL/6J mice exposed to SR, bulk GCaMP6 fibre photometry provided confirmatory in vivo evidence for engagement of int-BA-NAc neurons during social and sexual interactions. Therefore, populations of BA-NAc glutamate neurons are engaged by salient rewarding and aversive social stimuli in a topographic and valence-specific manner; this novel evidence is important to the overall understanding of the roles of this pathway in the circuitry of socio-emotional processing.

Social and non-social reward processing in subclinical depression.

This study applied two incentive delay tasks involving social and non-social incentive types to 76 pairs of participants with high and low depressive symptoms. The results suggest that higher levels of depressive symptoms are correlated with abnormalities in social and non-social reward processing even in the healthy populations.

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.

Sex differences in the impact of social status on social reward and associated mesolimbic activation.

Social stress plays an important role in the etiology of many neuropsychiatric disorders and can lead to a variety of behavioral deficits such as social withdrawal. One way that social stress may contribute to psychiatric disorders is by reducing social motivation and the rewarding properties of social interactions. We investigated the impact of social stress on social reward in the context of winning versus losing agonistic encounters in Syrian hamsters (Mesocricetus auratus). First, we tested the hypothesis that social stress resulting from either stable low, or subordinate, social status or from social defeat reduces the rewarding properties of social interactions. Using an Operant Social Preference (OSP) task to measure social reward/motivation, we found that both subordinate and socially defeated males made significantly fewer entries into chambers containing novel, same-sex conspecifics compared to males who were dominant (i.e., stably won the agonistic encounters). In females, however, there were no differences in social entries between winners and losers. In a second experiment, we found more activation of the mesolimbic dopamine system (MDS) as assessed with cFos immunohistochemistry in the lateral ventral tegmental area (lVTA) and the nucleus accumbens (NAc) shell of male winners compared to losers. In females, however, there were no differences in activation in the lVTA between winners and losers. Surprisingly, however, winning females displayed significantly more activation in the NAc shell as compared to losing females, despite the lack of behavioral differences. Thus, behavioral and histological data suggest that there are sex differences in the impact of social status on social reward and associated mesolimbic activation.

Early life social complexity shapes adult neural processing in the communal spiny mouse Acomys cahirinus.

RATIONALE: Early life social rearing has profound consequences on offspring behavior and resilience. Yet, most studies examining early life development in rodents use species whose young are born immobile and do not produce complex social behavior until later in development. Furthermore, models of rearing under increased social complexity, rather than deprivation, are needed to provide alternative insight into the development of social neural circuitry. OBJECTIVES: To understand precocial offspring social development, we manipulated early life social complexity in the communal spiny mouse Acomys cahirinus and assessed long-term consequences on offspring social behavior, exploration, and neural responses to novel social stimuli. METHODS: Spiny mouse pups were raised in the presence or absence of a non-kin breeding group. Upon adulthood, subjects underwent social interaction tests, an open field test, and a novel object test. Subjects were then exposed to a novel conspecific and novel group and neural responses were quantified via immunohistochemical staining in brain regions associated with social behavior. RESULTS: Early life social experience did not influence behavior in the test battery, but it did influence social processing. In animals exposed to non-kin during development, adult lateral septal neural responses toward a novel conspecific were weaker and hypothalamic neural responses toward a mixed-sex group were stronger. CONCLUSIONS: Communal species may exhibit robust behavioral resilience to the early life social environment. But the early life environment can affect how novel social information is processed in the brain during adulthood, with long-term consequences that are likely to shape their behavioral trajectory.

The effect of intranasal oxytocin on social reward processing in humans: a systematic review.

Understanding the neurobiology of social reward processing is fundamental, holding promises for reducing maladaptive/dysfunctional social behaviors and boosting the benefits associated with a healthy social life. Current research shows that processing of social (vs. non-social) rewards may be driven by oxytocinergic signaling. However, studies in humans often led to mixed results. This review aimed to systematically summarize available experimental results that assessed the modulation of social reward processing by intranasal oxytocin (IN-OXY) administration in humans. The literature search yielded 385 results, of which 19 studies were included in the qualitative synthesis. The effects of IN-OXY on subjective, behavioral, and (neuro)physiological output variables are discussed in relation to moderating variables-reward phase, reward type, onset and dosage, participants' sex/gender, and clinical condition. Results indicate that IN-OXY is mostly effective during the consumption ("liking") of social rewards. These effects are likely exerted by modulating the activity of the prefrontal cortex, insula, precuneus, anterior cingulate cortex, amygdala, and striatum. Finally, we provide suggestions for designing future oxytocin studies. Systematic review registration: https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42021278945, identifier CRD42021278945.

Improving social reward responsivity and social connectedness in psychotherapies for late-life depression: Engage & Connect as an example.

Psychotherapies are effective in reducing late-life depression. Yet, about half of patients remain depressed at treatment end. Advances in neuroscience can inform simplified interventions that target key brain networks impacted by depression. Behavioral activation therapies that increase social connectedness may improve social reward responsivity and alter abnormalities of the Positive Valence System (PVS). Engage & Connect is an example for a scalable and simple neuroscience-informed psychotherapy, aimed to improve PVS functions and social reward responsivity by increasing engagement in rewarding social activities. Interventions that improve social reward responsivity can be promising first-line treatments for late-life depression in the community.