Altered reward network responses to social touch in major depression

Introduction: Affective touch is highly rewarding and an integral part of social relationships. Major depressive disorder (MDD) is characterized by severe impairments in reward processing, but the neural effects of social touch in MDD are still elusive. Objective: We aimed to determine whether the neural processing of social touch is impaired in MDD and to assess the impact of antidepressant therapy. Methods: Before and after antidepressant treatment, 53 MDD patients and 41 healthy controls underwent functional magnetic resonance imaging (fMRI) while receiving social touch. We compared neural responses to social touch in the reward network, behavioral ratings of touch comfort and general aversion to interpersonal touch in MDD patients to controls. Additionally, we examined the effect of treatment response on those measures. Results: Clinical symptoms decreased after treatment and 43.4% of patients were classified as responders. Patients reported higher aversion to social touch and lower comfort ratings during the fMRI paradigm than controls. Patients showed reduced responses to social touch in the nucleus accumbens, caudate nucleus and putamen than controls, both before and after treatment. Non-responders exhibited blunted response in the caudate nucleus and the insula compared to responders, again irrespective of treatment. Conclusions: These findings confirm our hypothesis that interpersonal touch as an indicator of social reward processing is impaired in MDD. Persistent dysfunctional processing of social touch despite clinical improvements may constitute a latent risk factor for social withdrawal and isolation. New treatment approaches are necessary to specifically target social reward processing and disturbed body awareness in MDD.

Are conspecific social videos rewarding to chimpanzees (Pan troglodytes)? A test of the social motivation theory

Many claim that social stimuli are rewarding to primates, but few, if any, studies have explicitly demonstrated their reward value. Here, we examined whether chimpanzees would produce overt responses for the opportunity to view conspecific social, compared to dynamic (video: Experiment 1) and static (picture: Experiment 2) control content. We also explored the relationships between variation in social reward and social behavior and cognition. We provided captive chimpanzees with access to a touchscreen during four, one-hour sessions (two ‘conspecific social’ and two ‘control’). The sessions consisted of ten, 15-second videos (or pictures in Experiment 2) of either chimpanzees engaging in a variety of behaviors (social condition) or vehicles, humans, or other animals engaged in some activity (control condition). For each chimpanzee, we recorded the number of responses to the touchscreen and the frequency of watching the stimuli. Independent t-tests revealed no sex or rearing differences in touching and watching the social or control videos (p>0.05). Repeated measures ANOVAs showed chimpanzees touched and watched the screen significantly more often during the social compared to control video sessions. Furthermore, although chimpanzees did not touch the screen more often during social than control picture sessions in Experiment 2, they did watch the screen more often. Additionally, chimpanzees that previously performed better on a task of social cognition and engaged in more affiliative behavior watched a higher percentage of social videos during the touchscreen task. These results are consistent with the social motivation theory, and indicate social stimuli are intrinsically rewarding, as chimpanzees made more overt responses for the opportunity to view conspecific social, compared to control, content.

Can the reward associated with gaze leading train faster gaze shifts to a jointly attended target?

We investigated whether the reward that has previously been associated with initiated joint attention (the experience of having one’s gaze followed by someone else; Pfeiffer et al., 2014, Schilbach et al., 2010) can influence gaze behaviour and, similarly to monetary rewards (Blaukopf & DiGirolamo, 2005; Manohar et al., 2017; Milstein & Dorris, 2007), elicit learning effects. To this end, we adapted Milstein and Dorris (2007) gaze contingent paradigm, so it required participants to look at an anthropomorphic avatar and then conduct a saccade towards the left or right peripheral target. If participants were fast enough, they could experience social reward in terms of the avatar looking at the same target as they did and thus engaging with them in joint attention. One side had higher reward probability than the other (80 % vs 20 %; on the other fast trials the avatar would simply keep staring ahead). We expected that if participants learned about the reward contingency and if they found the experience of having their gaze followed rewarding, their latency and success rate would improve for saccades to the high rewarded targets. Although our current study did not demonstrate that such social reward has a long lasting effect on gaze behaviour, we found that latencies became shorter over time and that latencies were longer on congruent trials (target location was identical to the previous trial) than on noncongruent trials (target location different than on the previous trial), which could reflect inhibition of return.

Social selectivity and social motivation in voles

Selective relationships are fundamental to humans and many other animals, but relationships between mates, family members, or peers may be mediated differently. We examined connections between social reward and social selectivity, aggression, and oxytocin receptor signaling pathways in rodents that naturally form enduring, selective relationships with mates and peers (monogamous prairie voles) or peers (group-living meadow voles). Female prairie and meadow voles worked harder to access familiar vs. unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles displayed strongly selective huddling preferences for familiar animals, but only worked harder to repeatedly access females vs. males, with no difference in effort by familiarity. This reveals a striking sex difference in pathways underlying social monogamy, and demonstrates a fundamental disconnect between motivation and social selectivity in males-a distinction not detected by the partner preference test. Meadow voles exhibited social preferences but low social motivation, consistent with tolerance rather than reward supporting social groups in this species. Natural variation in oxytocin receptor binding predicted individual variation in prosocial and aggressive behaviors. These results provide a basis for understanding species, sex, and individual differences in the mechanisms underlying the role of social reward in social preference.

Examining Individual Differences in Social Reward Valuation: a Person-Based Approach

Social reward refers to the motivational and pleasurable aspects of our interactions with other people. While some people experience social encounters as pleasurable, others experience them as aversive. However, the current knowledge on individual differences in social reward valuation in relation to pro- and antisocial personality characteristics is limited. The Social Reward Questionnaire (SRQ) was developed to assess individual differences in the value of different types of social rewards. First, the present study examined the validity and reliability of the Dutch version of the SRQ in a Dutch and Flemish community sample (N = 1892). Second, using latent profile analysis (LPA), it was investigated whether subgroups of participants existed with distinctive patterns of social reward valuation, and whether these subgroups differed in their level of psychopathic traits, aggression, and social anxiety. The results confirmed the original six-factor structure and showed good reliability and validity. The LPA identified four classes of individuals, labelled as: Low Social Interest, High Social Interest, Undifferentiated Social Reward-seekers, and Socially Cruel. These classes were further typified by distinct levels of psychopathy, reactive and proactive aggression, and social anxiety. The present findings contribute to our understanding of individual variability in the underlying motives of social behaviors.

Reduced motivation for social contact in Disrupted-in-schizophrenia transgenic rats

The Disrupted-in-schizophrenia 1 (DISC1) signaling pathway is considered to play a key role in schizophrenia, depression, autism and other psychiatric disorders. DISC1 is involved in regulating the dopaminergic neurotransmission in, among others, the mesolimbic reward system. A transgenic rat line tgDISC1 has been introduced as a model system to study behavioral phenotypes associated with abnormal DISC1 pathways. Here, we evaluated the impact of impaired DISC1 signaling on social (social interaction) and non-social (sucrose) reward preferences in the tgDISC1 animal model. In a plus-maze setting, rats chose between the opportunity for social interaction with an unfamiliar juvenile conspecific (social reward) or drinking sweet solutions with variable sucrose concentrations (non-social reward). tgDISC1 rats differed from wild-type rats in their social, but not in their non-social reward preferences. Specifically, DISC1 rats showed a lower interest in interaction with the juvenile conspecific, but did not differ from wild-type rats in their preference for higher sucrose concentrations. These results suggest that disruptions of the DISC1 pathway that is associated with altered dopamine transmission in the brain result in selective deficits in social motivation seen in neuropsychiatric illness.

MDMA-Assisted Therapy as a Means to Alter Affective, Cognitive, Behavioral, and Neurological Systems Underlying Social Dysfunction in Social Anxiety Disorder

Social anxiety disorder (SAD) is a prevalent and often debilitating psychiatric disorder that can assume a chronic course even when treated. Despite the identification of evidence-based pharmacological and behavioral treatments for SAD, much room for improved outcomes exists and 3,4-methylenedioxymethamphetamine (MDMA) has been proposed as a promising adjunctive treatment to psychological interventions for disorders characterized by social dysfunction. A small randomized, placebo-controlled trial of MDMA-assisted therapy (MDMA-AT) for social anxiety in autistic adults offered encouraging results, but more research is sorely needed to explore the potential for MDMA-AT in treating SAD. This review aims to stimulate future study by summarizing research on disruptions in neurological, perceptual, receptive, and expressive systems regulating social behavior in SAD and proposing how MDMA-AT may alter these systems across four domains. First, we review research highlighting the roles of social anhedonia and reduced social reward sensitivity in maintaining SAD, with specific attention to the reduction in positive affect in social situations, infrequent social approach behaviors, and related social skills deficits. We posit that MDMA-AT may enhance motivation to connect with others and alter perceptions of social reward for an extended period following administration, thereby potentiating extinction processes, and increasing the reinforcement value of social interactions. Second, we review evidence for the central role of heightened social evaluative threat perception in the development and maintenance of SAD and consider how MDMA-AT may enhance experiences of affiliation and safety when interacting with others. Third, we consider the influence of shame and the rigid application of shame regulation strategies as important intrapersonal processes maintaining SAD and propose the generation of self-transcendent emotions during MDMA sessions as a mechanism of shame reduction that may result in corrective emotional experiences and boost memory reconsolidation. Finally, we review research on the role of dysfunctional interpersonal behaviors in SAD that interfere with social functioning and, in particular, the development and maintenance of close and secure relationships. We discuss the hypothesized role of MDMA-AT in improving social skills to elicit positive interpersonal responses from others, creating a greater sense of belonging, acceptance, and social efficacy.

The angiotensin antagonist Losartan shifts social reward motivation and punishment sensitivity via modulating midbrain-striato-frontal circuits

Background Social deficits and dysregulations in dopaminergic midbrain-striato-frontal circuits represent transdiagnostic symptoms across psychiatric disorders. Animal models suggest that modulating interactions between the dopamine and renin-angiotensin system with the angiotensin receptor antagonist Losartan (LT) can modulate learning and reward-related processes. We have therefore determined the behavioral and neural effects of LT on social reward and punishment processing in humans. Methods A pre-registered randomized double-blind placebo-controlled between-subject pharmacological design was combined with a social incentive delay fMRI paradigm during which subjects could avoid social punishment or gain social reward. Healthy volunteers received a single-dose of LT (50mg, n=43) or placebo (n=44). Reaction times and emotional ratings served as behavioral outcomes, on the neural level activation, connectivity and social feedback prediction errors were modelled. Results Relative to placebo, LT switched reaction times and arousal away from prioritizing punishment towards social reward. On the neural level the LT-enhanced motivational salience of social rewards was accompanied by stronger ventral striatum-prefrontal connectivity during reward anticipation and attenuated activity in the ventral tegmental area (VTA) and associated connectivity with the bilateral insula in response to punishment during the outcome phase. Computational modelling further revealed an LT-enhanced social reward prediction error signal in VTA and dorsal striatum. Conclusions LT shifted motivational and emotional salience away from social punishment towards social reward via modulating distinct core nodes of the midbrain-striato-frontal circuits. The findings document a modulatory role of the renin-angiotensin system in these circuits and associated social processes, suggesting a promising treatment target to alleviate social dysregulations.