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.

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.

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.

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.

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.

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 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.

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.

Reward learning improves social signal processing in autism model mice.

Social and reward signal processing and their association are critical elements of social motivation. Despite the use of reward learning to improve the social interactions of patients with autism spectrum disorder (ASD), the underlying neural mechanisms are unknown. Here, we found different yet conjunct neuronal representations of social and reward signals in the mouse medial prefrontal cortex (mPFC). We also found that social signal processing is selectively disrupted, whereas reward signal processing is intact in the mPFC of Shank2-knockout mice, a mouse model of ASD. Furthermore, reward learning not only allows Shank2-knockout mice to associate social stimuli with reward availability, but it also rescues the impaired social signal processing. These findings provide insights into the neural basis for the therapeutic use of reward learning in ASD.

Remembering unexpected beauty: Contributions of the ventral striatum to the processing of reward prediction errors regarding the facial attractiveness in face memory.

The COVID-19 pandemic has led people to predict facial attractiveness from partially covered faces. Differences in the predicted and observed facial attractiveness (i.e., masked and unmasked faces, respectively) are defined as reward prediction error (RPE) in a social context. Cognitive neuroscience studies have elucidated the neural mechanisms underlying RPE-induced memory improvements in terms of monetary rewards. However, little is known about the mechanisms underlying RPE-induced memory modulation in terms of social rewards. To elucidate this, the present functional magnetic resonance imaging (fMRI) study investigated activity and functional connectivity during face encoding. In encoding trials, participants rated the predicted attractiveness of faces covered except for around the eyes (prediction phase) and then rated the observed attractiveness of these faces without any cover (outcome phase). The difference in ratings between these phases was defined as RPE in facial attractiveness, and RPE was categorized into positive RPE (increased RPE from the prediction to outcome phases), negative RPE (decreased RPE from the prediction to outcome phases), and non-RPE (no difference in RPE between the prediction and outcome phases). During retrieval, participants were presented with individual faces that had been seen and unseen in the encoding trials, and were required to judge whether or not each face had been seen in the encoding trials. Univariate activity in the ventral striatum (VS) exhibited a linear increase with increased RPE in facial attractiveness. In the multivariate pattern analysis (MVPA), activity patterns in the VS and surrounding areas (extended VS) significantly discriminated between positive/negative RPE and non-RPE. In the functional connectivity analysis, significant functional connectivity between the extended VS and the hippocampus was observed most frequently in positive RPE. Memory improvements by face-based RPE could be involved in functional networks between the extended VS (representing RPE) and the hippocampus, and the interaction could be modulated by RPE values in a social context.

The Relevance of Animal Models of Social Isolation and Social Motivation for Understanding Schizophrenia: Review and Future Directions.

BACKGROUND AND HYPOTHESES: Social dysfunction in schizophrenia includes symptoms of withdrawal and deficits in social skills, social cognition, and social motivation. Based on the course of illness, with social withdrawal occurring prior to psychosis onset, it is likely that the severity of social withdrawal/isolation contributes to schizophrenia neuropathology. STUDY DESIGN: We review the current literature on social isolation in rodent models and provide a conceptual framework for its relationship to social withdrawal and neural circuit dysfunction in schizophrenia. We next review preclinical tasks of social behavior used in schizophrenia-relevant models and discuss strengths and limitations of existing approaches. Lastly, we consider new effort-based tasks of social motivation and their potential for translational studies in schizophrenia. STUDY RESULTS: Social isolation rearing in rats produces profound differences in behavior, pharmacologic sensitivity, and neurochemistry compared to socially reared rats. Rodent models relevant to schizophrenia exhibit deficits in social behavior as measured by social interaction and social preference tests. Newer tasks of effort-based social motivation are being developed in rodents to better model social motivation deficits in neuropsychiatric disorders. CONCLUSIONS: While experimenter-imposed social isolation provides a viable experimental model for understanding some biological mechanisms linking social dysfunction to clinical and neural pathology in schizophrenia, it bypasses critical antecedents to social isolation in schizophrenia, notably deficits in social reward and social motivation. Recent efforts at modeling social motivation using effort-based tasks in rodents have the potential to quantify these antecedents, identify models (eg, developmental, genetic) that produce deficits, and advance pharmacological treatments for social motivation.

Social reward processing in depressed and healthy individuals across the lifespan: A systematic review and a preliminary coordinate-based meta-analysis of fMRI studies.

BACKGROUND: Social rewards (e.g., social feedback, praise, and social interactions) are fundamental to social learning and relationships across the life span. Exposure to social rewards is linked to activation in key brain regions, that are impaired in major depression. This is the first summary of neuroimaging literature on social reward processing in depressed and healthy individuals. METHOD: We screened 409 studies and identified 25 investigating task-based fMRI activation during exposure to social stimuli in depressed and healthy populations across the lifespan. We conducted a systematic review followed by an Activation Likelihood Estimation (ALE) analysis of three main contrasts: a) positive social feedback vs. neutral stimuli; b) negative social feedback vs. neutral stimuli; c) positive vs. negative social feedback. We also compared activation patterns in depressed versus healthy controls. RESULTS: Systematic review revealed that social rewards elicit increased activation in subcortical reward regions (NAcc, amygdala, ventral striatum, thalamus) in healthy and depressed individuals; and decreased activation in prefrontal reward regions (medial prefrontal cortex, orbitofrontal cortex) among depressed persons. Our meta-analysis showed, in both depressed and healthy individuals, increased cluster activation of the putamen and caudate in response to negative social stimuli vs. positive stimuli. We also found increased cluster activation in the inferior frontal gyrus (IFG) and the medial frontal gyrus (MFG) in healthy controls vs. depressed individuals, in response to negative social stimuli. CONCLUSIONS: Processing of social stimuli elicits activation of key brain regions involved in affective and social information processing. Interventions for depression can increase social reward responsivity to improve outcomes.

The motivation to flock correlates with vocal-social behaviors and dopamine-related gene expression in male European starlings.

It is proposed that songbird flocks are partly reinforced by positive social interactions, however not all flock mate interactions are positive. The combination of both positive and negative social interactions with flock mates may play a role in the motivation for birds to flock. The nucleus accumbens (NAc), medial preoptic area (POM), and ventral tegmental area (VTA) are implicated in vocal-social behaviors in flocks, including singing. Dopamine (DA) within these regions modifies motivated, reward-directed behaviors. Here, we begin to test the hypothesis that individual social interactions and DA within these regions are involved in the motivation to flock. Vocal-social behaviors were recorded in eighteen male European starlings in mixed-sex flocks in fall, when starlings are highly social and form large flocks. Males were then singly removed from their flock and the motivation to flock was quantified as the amount of time spent attempting to join a flock following separation. We used quantitative real-time polymerase chain reaction to measure expression of DA-related genes in the NAc, POM, and VTA. Birds producing high levels of vocal behaviors were more highly motivated to flock and had higher tyrosine hydroxylase (the rate-limiting enzyme in DA synthesis) expression in the NAc and VTA. Birds that received high levels of agonistic behaviors were less motivated to flock and had higher DA receptor subtype 1 expression in the POM. Overall, our findings suggest that interplay between social experience and DA activity in NAc, POM, and VTA plays a key role in social motivation in flocking songbirds.