Social Reward Anticipation Research Articles

Examining the value of body gestures in social reward contexts

Brain regions associated with the processing of tangible rewards (such as money, food, or sex) are also involved in anticipating social rewards and avoiding social punishment. To date, studies investigating the neural underpinnings of social reward have presented feedback via static or dynamic displays of faces to participants. However, research demonstrates that participants find another type of social stimulus, namely, biological motion, rewarding as well, and exert effort to engage with this type of stimulus. Here we examine whether feedback presented via body gestures in the absence of facial cues also acts as a rewarding stimulus and recruits reward-related brain regions. To achieve this, we investigated the neural underpinnings of anticipating social reward and avoiding social disapproval presented via gestures alone, using a social incentive delay task. As predicted, the anticipation of social reward and avoidance of social disapproval engaged reward-related brain regions, including the nucleus accumbens, in a manner similar to previous studies’ reports of feedback presented via faces and money. This study provides the first evidence that human body motion alone engages brain regions associated with reward processing in a similar manner to other social (i.e. faces) and non-social (i.e. money) rewards. The findings advance our understanding of social motivation in human perception and behavior.

T228. SOCIAL REWARD REACTIVITY AND SENSITIVITY IN SCHIZOPHRENIA SPECTRUM CONDITIONS

BackgroundIndividuals with schizophrenia spectrum disorders often experience less pleasure during social interaction and frequently demonstrate reduced social motivation. This research examines the extent to which these behaviours may be linked to reduced social reward reactivity and sensitivity, and aims to clarify whether schizophrenia spectrum traits are associated with reduced behavioural and neural responsiveness to social rewards. It includes a systematic review and meta-analyses of social reward sensitivity research in schizophrenia, and also provides preliminary data (participant n = 50) on a novel avatar-based social incentive delay task that was created to further investigate the links between schizophrenia spectrum traits and social reward reactivity.MethodsFirst, a systematic review and meta-analyses (literature database search conducted November 2019) found six studies that investigated social reward anticipation and consumption within the schizophrenia continuum (total participant n = 440). Four investigated social reward sensitivity in clinical samples with schizophrenia diagnoses, and two studied the links between social anhedonia traits and social reward responding in normative samples. The novel social incentive delay task presents participants with the opportunity to win animated avatar-based monetary or social rewards by responding to a cued target.ResultsThe narrative review and meta-analyses of behavioural data from clinical and normative samples found that individuals with schizophrenia diagnoses or traits demonstrate significantly reduced behavioural anticipation of social rewards in comparison to healthy controls. Furthermore, this reduced reward reactivity was more pronounced for social rewards than for monetary rewards. This effect was also mirrored at neural levels, with individuals with schizophrenia demonstrating reduced social reward-related activation in areas such as the ventral striatum and anterior cingulate cortex. Preliminary behavioural data from the social incentive delay task suggest that, in normative samples, more pronounced negative schizotypal traits are associated with reduced anticipation and consumption of social rewards. Like in the reviewed studies, this reduced anticipation was more marked for social rewards than for monetary rewards.DiscussionThis research suggests that schizophrenia spectrum traits are associated with reduced reactivity and sensitivity to social rewards. It also highlights that this reduced reactivity is demonstrated at behavioural and neural levels, and is more marked for social rewards than for monetary rewards. We consider the implications of these findings for treatment programmes that target atypical social behaviour within schizophrenia spectrum conditions. A series of methodological recommendations for future work investigating social reward reactivity in schizophrenia are also included.

P.231 Social withdrawal levels influence cerebellar activity during anticipation of social rewards: a trans-diagnostic result

P.231 Social withdrawal levels influence cerebellar activity during anticipation of social rewards: a trans-diagnostic result

Facial responses of adult humans during the anticipation and consumption of touch and food rewards

Whether cognitive, motivational and hedonic aspects of reward anticipation and consumption can be reliably assessed with explicit and implicit measures, and if different motivational (decision utility) and hedonic (experienced utility) processes get recruited by distinct reward types, remain partly unsolved questions that are relevant for theories of social and non-social decision-making. We investigated these topics using a novel experimental paradigm, including carefully matched social and nonsocial rewards, and by focusing on facial responses. Facial expressions are indeed an often-cited implicit measure of rewards’ hedonic impact. For example, food rewards elicit powerful facial responses – characterized by lip smacking, tongue protrusion, and relaxation of the middle face – in human newborns, juvenile monkeys, and adult rats. The same stimuli elicit more nuanced facial reactions in adult humans, which can be best captured with facial electromyography (fEMG). However, little is known about facial expressions preceding reward consumption, reflecting the motivation to obtain and possibly the expected pleasantness of a reward, and whether similar facial expressions are elicited by different types of rewards. To investigate these questions, a novel within-subject experimental paradigm was developed. During the anticipation and consumption of social (affective touch) and nonsocial (food) rewards, explicit (ratings of wanting and liking, physical effort) and implicit (fEMG) measures of wanting and liking were taken in 43 healthy adult participants. Reduced activation of the Corrugator Supercilii (CS) muscle (reflecting less frowning and indicating greater positive response) was found in trials with higher wanting and effort during the anticipation of food rewards, as well as in trials with higher liking and effort during the consumption of food rewards. The CS muscle is thus a sensitive measure of wanting and liking of food rewards both during their anticipation and consumption. Crucially, thanks to careful reward matching, these results cannot be explained by differences in subjective wanting, liking, or effort produced to obtain the two types of rewards. No significant modulation of the Zygomaticus Major (ZM) muscle was found for social or food rewards. Explorative analyses however indicated that the ZM may activate during the delivery of the most wanted touch, but not for the most wanted food. The absence of significant effects of social rewards on the activation of CS and ZM muscles are discussed in relation to the specifics of this innovative task comparing two types of matched rewards in the same participants. The present findings contribute to the understanding of the processes underlying motivational and hedonic aspects of rewards, and may therefore inform models of social and non-social decision-making.

The effects of intranasal oxytocin on reward circuitry responses in children with autism spectrum disorder

BackgroundIntranasal oxytocin (OT) has been shown to improve social communication functioning of individuals with autism spectrum disorder (ASD) and, thus, has received considerable interest as a potential ASD therapeutic agent. Although preclinical research indicates that OT modulates the functional output of the mesocorticolimbic dopamine system that processes rewards, no clinical brain imaging study to date has examined the effects of OT on this system using a reward processing paradigm. To address this, we used an incentive delay task to examine the effects of a single dose of intranasal OT, versus placebo (PLC), on neural responses to social and nonsocial rewards in children with ASD.MethodsIn this placebo-controlled double-blind study, 28 children and adolescents with ASD (age: M = 13.43 years, SD = 2.36) completed two fMRI scans, one after intranasal OT administration and one after PLC administration. During both scanning sessions, participants completed social and nonsocial incentive delay tasks. Task-based neural activation and connectivity were examined to assess the impact of OT relative to PLC on mesocorticolimbic brain responses to social and nonsocial reward anticipation and outcomes.ResultsCentral analyses compared the OT and PLC conditions. During nonsocial reward anticipation, there was greater activation in the right nucleus accumbens (NAcc), left anterior cingulate cortex (ACC), bilateral orbital frontal cortex (OFC), left superior frontal cortex, and right frontal pole (FP) during the OT condition relative to PLC. Alternatively, during social reward anticipation and outcomes, there were no significant increases in brain activation during the OT condition relative to PLC. A Treatment Group × Reward Condition interaction revealed relatively greater activation in the right NAcc, right caudate nucleus, left ACC, and right OFC during nonsocial relative to social reward anticipation during the OT condition relative to PLC. Additionally, these analyses revealed greater activation during nonsocial reward outcomes during the OT condition relative to PLC in the right OFC and left FP. Finally, functional connectivity analyses generally revealed changes in frontostriatal connections during the OT condition relative to PLC in response to nonsocial, but not social, rewards.ConclusionsThe effects of intranasal OT administration on mesocorticolimbic brain systems that process rewards in ASD were observable primarily during the processing of nonsocial incentive salience stimuli. These findings have implications for understanding the effects of OT on neural systems that process rewards, as well as for experimental trials of novel ASD treatments developed to ameliorate social communication impairments in ASD.

Hypernatural Monitoring: A Social Rehearsal Account of Smartphone Addiction.

We present a deflationary account of smartphone addiction by situating this purportedly antisocial phenomenon within the fundamentally social dispositions of our species. While we agree with contemporary critics that the hyper-connectedness and unpredictable rewards of mobile technology can modulate negative affect, we propose to place the locus of addiction on an evolutionarily older mechanism: the human need to monitor and be monitored by others. Drawing from key findings in evolutionary anthropology and the cognitive science of religion, we articulate a hypernatural monitoring model of smartphone addiction grounded in a general social rehearsal theory of human cognition. Building on recent predictive-processing views of perception and addiction in cognitive neuroscience, we describe the role of social reward anticipation and prediction errors in mediating dysfunctional smartphone use. We conclude with insights from contemplative philosophies and harm-reduction models on finding the right rituals for honoring social connections and setting intentional protocols for the consumption of social information.

Blunted cardiovascular reactivity during social reward anticipation in subclinical depression

The present study extends past research about reduced reward responsiveness in depression by assessing effort-related cardiovascular responses during anticipation of a social reward. Dysphoric (i.e., subclinically depressed) and nondysphoric participants worked on a cognitive task. Half the participants in each group expected the possibility to subscribe to a social exchange internet site. Effort mobilization during task performance was assessed by participants' cardiovascular reactivity. Confirming the predictions, nondysphoric participants in the social-reward condition had higher reactivity of pre-ejection period, systolic blood pressure, and heart rate, compared to the other three cells. In contrast, dysphoric participants' cardiovascular reactivity was generally low. These findings indicate that social-reward function is indeed impaired in subclinical depression. Implications for social punishment are discussed.

Anticipation of Social and Monetary Rewards in Schizophrenia

Numerous behavioural and neuroimaging studies have explored human cognitive processing of various rewards, such as food, monetary or social stimuli. Previous studies with patients suffering from schizophrenia (SZ) used incentive delay tasks with monetary rewards. Apart from slower reaction times in general in SZ, there were no differences in task performance between patients with schizophrenia and healthy controls (HC). Patients with schizophrenia have impaired social functioning and thus may have a disturbed sensitivity to social rewards. 54 schizophrenia patients and 54 matched healthy controls completed a reward paradigm (incentive delay task) with monetary (MID) and social stimuli (SID). Reaction times and hit rates were analysed using a three-way repeated measures ANOVA. Patients demonstrated increased reaction times in both, the MID and the SID tasks compared to health controls. Hit rates for healthy controls significantly increased in the MID task, however these results were not found in the SID task with increasing reward level. In both tasks SZ improved their performance as rewards increased. The present findings suggest that patients with SZ are capable to anticipate monetary or social rewards and use this anticipation to guide their behaviour. Extrapolated to social functioning, the capability to anticipate potential reward could be used in therapeutic interventions.

Effects of alexithymia and empathy on the neural processing of social and monetary rewards.

Empathy has been found to affect the neural processing of social and monetary rewards. Alexithymia, a subclinical condition showing a close inverse relationship with empathy is linked to dysfunctions of socio-emotional processing in the brain. Whether alexithymia alters the neural processing of rewards, which is currently unknown. Here, we investigated the influence of both alexithymia and empathy on reward processing using a social incentive delay (SID) task and a monetary incentive delay (MID) task in 45 healthy men undergoing functional magnetic resonance imaging. Controlling for temperament-character dimensions and rejection sensitivity, the relationship of alexithymia and empathy with neural activity in several a priori regions of interest (ROIs) was examined by means of partial correlations, while participants anticipated and received social and monetary rewards. Results were considered significant if they survived Holm-Bonferroni correction for multiple comparisons. Alexithymia modulated neural activity in several ROIs of the emotion and reward network, both during the anticipation of social and monetary rewards and in response to the receipt of monetary rewards. In contrast, empathy did not affect reward anticipation and modulated ROI activity only in response to the receipt of social rewards. These results indicate a significant influence of alexithymia on the processing of social and monetary rewards in the healthy brain.

Spatiotemporal dissociation of brain activity underlying threat and reward in social anxiety disorder.

Social anxiety disorder (SAD) involves abnormalities in social motivation, which may be independent of well-documented differences in fear and arousal systems. Yet, the neurobiology underlying motivational difficulties in SAD is not well understood. The aim of the current study was to spatiotemporally dissociate reward circuitry dysfunction from alterations in fear and arousal-related neural activity during anticipation and notification of social and non-social reward and punishment. During fMRI acquisition, non-depressed adults with social anxiety disorder (SAD; N = 21) and age-, sex- and IQ-matched control subjects (N = 22) completed eight runs of an incentive delay task, alternating between social and monetary outcomes and interleaved in alternating order between gain and loss outcomes. Adults with SAD demonstrated significantly reduced neural activity in ventral striatum during the anticipation of positive but not negative social outcomes. No differences between the SAD and control groups were observed during anticipation of monetary gain or loss outcomes or during anticipation of negative social images. However, consistent with previous work, the SAD group demonstrated amygdala hyper-activity upon notification of negative social outcomes. Degraded anticipatory processing in bilateral ventral striatum in SAD was constrained exclusively to anticipation of positive social information and dissociable from the effects of negative social outcomes previously observed in the amygdala. Alterations in anticipation-related neural signals may represent a promising target for treatment that is not addressed by available evidence-based interventions, which focus primarily on fear extinction and habituation processes.

Gender-specific modulation of neural mechanisms underlying social reward processing by Autism Quotient.

Autism spectrum disorder refers to a neurodevelopmental condition primarily characterized by deficits in social cognition and behavior. Subclinically, autistic features are supposed to be present in healthy humans and can be quantified using the Autism Quotient (AQ). Here, we investigated a potential relationship between AQ and neural correlates of social and monetary reward processing, using functional magnetic resonance imaging in young, healthy participants. In an incentive delay task with either monetary or social reward, reward anticipation elicited increased ventral striatal activation, which was more pronounced during monetary reward anticipation. Anticipation of social reward elicited activation in the default mode network (DMN), a network previously implicated in social processing. Social reward feedback was associated with bilateral amygdala and fusiform face area activation. The relationship between AQ and neural correlates of social reward processing varied in a gender-dependent manner. In women and, to a lesser extent in men, higher AQ was associated with increased posterior DMN activation during social reward anticipation. During feedback, we observed a negative correlation of AQ and right amygdala activation in men only. Our results suggest that social reward processing might constitute an endophenotype for autism-related traits in healthy humans that manifests in a gender-specific way.

Event-related EEG responses to anticipation and delivery of monetary and social reward

Monetary and a social incentive delay tasks were used to characterize reward anticipation and delivery with electroencephalography. During reward anticipation, N1, P2 and P3 components were modulated by both prospective reward value and incentive type (monetary or social), suggesting distinctive allocation of attentional and motivational resources depending not only on whether rewards or non-rewards were cued, but also on the monetary and social nature of the prospective outcomes. In the delivery phase, P2, FRN and P3 components were also modulated by levels of reward value and incentive type, illustrating how distinctive affective and cognitive processes were attached to the different outcomes. Our findings imply that neural processing of both reward anticipation and delivery can be specific to incentive type, which might have implications for basic as well as translational research. These results are discussed in the light of previous electrophysiological and neuroimaging work using similar tasks.

Diminished social reward anticipation in the broad autism phenotype as revealed by event-related brain potentials.

Diminished responsivity to reward incentives is a key contributor to the social-communication problems seen in autism spectrum disorders (ASDs). Social motivation theories suggest that individuals with ASD do not experience social interactions as rewarding, leading to negative consequences for the development of brain circuitry subserving social information. In this study, we examined neural responses to social and non-social reward anticipation in 35 typically developing young adults, examining modulation of reward sensitivity by level of autistic traits. Using an Event-related potential incentive-delay task incorporating novel, more ecologically valid forms of reward, higher expression of autistic traits was associated with an attenuated P3 response to the anticipation of social (simulated real-time video feedback from an observer), but not non-social (candy), rewards. Exploratory analyses revealed that this was unrelated to mentalizing ability. The P3 component reflects motivated attention to reward signals, suggesting attenuated motivation allocation specific to social incentives. The study extends prior findings of atypical reward anticipation in ASD, demonstrating that attenuated social reward responsiveness extends to autistic traits in the range of typical functioning. Results support the development of innovative paradigms for investigating social and non-social reward responsiveness. Insight into vulnerabilities in reward processing is critical for understanding social function in ASD.

Doing good or bad: How interactions between action and emotion expectations shape the sense of agency

The emotional consequences of our own and others’ actions can influence our agentive self-awareness in social contexts. Positive outcomes are usually linked to the self and used for self-enhancement, whereas negative outcomes are more often attributed to others. In most situations, these causal attribution tendencies seem to be immediately present instead of involving reflective interpretations of the action experience. To address the question at which level of the cognitive hierarchy emotions and action perception interact, we adopted a social reward anticipation paradigm. Here, participants or their interaction partner received positive or negative action outcomes and performed speeded attribution choices regarding causation of the action outcome. Event-Related Potential (ERP) results showed that the emotional value of an outcome already influenced the classical N1 self-attenuation effect, with reduced embodied agentive self-awareness for negative outcomes at initial sensorimotor stages. At the level of the N300, the degree of updating and affective evaluation associated with the respective attributive decision was reflected and particularly associated to attribution tendencies for positive events. Our results show an early interaction between emotion and agency processes, and suggest that self-serving cognition can be grounded in embodied knowledge from low-level sensorimotor mechanisms.

Neural sensitivity to social reward and punishment anticipation in social anxiety disorder.

An imbalance in the neural motivational system may underlie Social Anxiety Disorder (SAD). This study examines social reward and punishment anticipation in SAD, predicting a valence-specific effect: increased striatal activity for punishment avoidance compared to obtaining a reward. Individuals with SAD (n = 20) and age, gender, and education case-matched controls (n = 20) participated in a functional magnetic resonance imaging (fMRI) study. During fMRI scanning, participants performed a Social Incentive Delay (SID) task to measure the anticipation of social reward and punishment. The left putamen (part of the striatum) showed a valence-specific interaction with group after correcting for medication use and comorbidity. The control group showed a relatively stronger activation for reward vs. punishment trials, compared to the social anxiety group. However, post-hoc pairwise comparisons were not significant, indicating that the effect is driven by a relative difference. A connectivity analysis (Psychophysiological interaction) further revealed a general salience effect: SAD patients showed decreased putamen-ACC connectivity compared to controls for both reward and punishment trials. Together these results suggest that the usual motivational preference for social reward is absent in SAD. In addition, cortical control processes during social incentive anticipation may be disrupted in SAD. These results provide initial evidence for altered striatal involvement in both valence-specific and valence-nonspecific processing of social incentives, and stress the relevance of taking motivational processes into account when studying social anxiety.

Lasting associations between early-childhood temperament and late-adolescent reward-circuitry response to peer feedback

Behavioral inhibition, a temperament identifiable in infancy, is associated with heightened withdrawal from social encounters. Prior studies raise particular interest in the striatum, which responds uniquely to monetary gains in behaviorally inhibited children followed into adolescence. Although behavioral manifestations of inhibition are expressed primarily in the social domain, it remains unclear whether observed striatal alterations to monetary incentives also extend to social contexts. In the current study, imaging data were acquired from 39 participants (17 males, 22 females; ages 16-18 years) characterized since infancy on measures of behavioral inhibition. A social evaluation task was used to assess neural response to anticipation and receipt of positive and negative feedback from novel peers, classified by participants as being of high or low interest. As with monetary rewards, striatal response patterns differed during both anticipation and receipt of social reward between behaviorally inhibited and noninhibited adolescents. The current results, when combined with prior findings, suggest that early-life temperament predicts altered striatal response in both social and nonsocial contexts and provide support for continuity between temperament measured in early childhood and neural response to social signals measured in late adolescence and early adulthood.

Differential patterns of nucleus accumbens activation during anticipation of monetary and social reward in young and older adults.

Recent studies have reported inconsistent results regarding the loss of reward sensitivity in the aging brain. Although such an age effect might be due to a decline of physiological processes, it may also be a consequence of age-related changes in motivational preference for different rewards. Here, we examined whether the age effects on neural correlates of reward anticipation are modulated by the type of expected reward. Functional magnetic resonance images were acquired in 24 older (60-78 years) and 24 young participants (20-28 years) while they performed an incentive delay task offering monetary or social rewards. Anticipation of either reward type recruited brain structures associated with reward, including the nucleus accumbens (NAcc). Region of interest analysis revealed an interaction effect of reward type and age group in the right NAcc: enhanced activation to cues of social reward was detected in the older subsample while enhanced activation to cues of monetary reward was detected in the younger subsample. Our results suggest that neural sensitivity to reward-predicting cues does not generally decrease with age. Rather, neural responses in the NAcc appear to be modulated by the type of reward, presumably reflecting age-related changes in motivational value attributed to different types of reward.

Common and distinct neural features of social and non-social reward processing in autism and social anxiety disorder

Autism spectrum disorders (ASDs) and social anxiety disorder (SAD) are both characterized by social dysfunction, but no study to date has compared neural responses to social rewards in ASDs and SAD. Neural responses during social and non-social reward anticipation and outcomes were examined in individuals with ASD (n = 16), SAD (n = 15) and a control group (n = 19) via functional magnetic resonance imaging. Analyses modeling all three groups revealed increased nucleus accumbens (NAc) activation in SAD relative to ASD during monetary reward anticipation, whereas both the SAD and ASD group demonstrated decreased bilateral NAc activation relative to the control group during social reward anticipation. During reward outcomes, the SAD group did not differ significantly from the other two groups in ventromedial prefrontal cortex activation to either reward type. Analyses comparing only the ASD and SAD groups revealed greater bilateral amygdala activation to social rewards in SAD relative to ASD during both anticipation and outcome phases, and the magnitude of left amygdala hyperactivation in the SAD group during social reward anticipation was significantly correlated with the severity of trait anxiety symptoms. Results suggest reward network dysfunction to both monetary and social rewards in SAD and ASD during reward anticipation and outcomes, but that NAc hypoactivation during monetary reward anticipation differentiates ASD from SAD.

Atypical Brain Responses to Reward Cues in Autism as Revealed by Event-Related Potentials

Social motivation deficit theories suggest that children with autism do not properly anticipate and appreciate the pleasure of social stimuli. In this study, we investigated event-related brain potentials evoked by cues that triggered social versus monetary reward anticipation in children with autism. Children with autism showed attenuated P3 activity in response to cues associated with a timely reaction to obtain a reward, irrespective of reward type. We attribute this atypical P3 activity in response to reward cues as reflective of diminished motivated attention to reward signals, a possible contributor to reduced social motivation in autism. Thus, our findings suggest a general reward processing deficit rather than a specific social reward dysfunction in autism.

Common alterations in sensitivity to type but not amount of reward in ADHD and autism spectrum disorders

Children with attention deficit/hyperactivity disorder (ADHD) display abnormalities in reward processing. Most reward studies have focused on the effects of material or monetary rewards. Studies with autism spectrum disorder (ASD) have focused on social rewards. In this study we compared the effects of amount and type of reward in children with ADHD and those with ASD. Two adapted versions of the Monetary Incentive Delay Task were used to study the effects of monetary and social reward anticipation on performance in 40 typically developing (TD) children and adolescents (8-16y), 35 children and adolescents with ADHD and 31 children and adolescents with ASD. Monetary and social reward improved accuracy and response time (RT) in all groups. The higher the anticipated reward, the more accurate and faster were responses. Independent of these effects, there was a differential effect of reward type. Both clinical groups, but not TD, responded faster for monetary than social rewards. The results, while not supporting hyposensitivity to changes in reward amount in ADHD and ASD, do suggest that both groups are generally less motivated in settings where social as opposed to monetary rewards can be earned.