Behavioral and Neural Dissociation of Social Anxiety and Loneliness.

Loneliness is a public health concern with detrimental effects on physical and mental well-being. Given phenotypical overlaps between loneliness and social anxiety (SA), cognitive-behavioral interventions targeting SA might be adopted to reduce loneliness. However, whether SA and loneliness share the same underlying neurocognitive mechanisms is still an elusive question. The current study aimed at investigating to what extent known behavioral and neural correlates of social avoidance in SA are evident in loneliness. We used a prestratified approach involving 42 (21 females) participants with high loneliness (HL) and 40 (20 females) participants with low loneliness (LL) scores. During fMRI, participants completed a social gambling task to measure the subjective value of engaging in social situations and responses to social feedback. Univariate and multivariate analyses of behavioral and neural data replicated known task effects. However, although HL participants showed increased SA, loneliness was associated with a response pattern clearly distinct from SA. Specifically, contrary to expectations based on SA differences, Bayesian analyses revealed moderate evidence for equal subjective values of engaging in social situations and comparable amygdala responses to social decision-making and striatal responses to positive social feedback in both groups. Moreover, while explorative analyses revealed reduced pleasantness ratings, increased striatal activity, and decreased striatal-hippocampal connectivity in response to negative computer feedback in HL participants, these effects were diminished for negative social feedback. Our findings suggest that, unlike SA, loneliness is not associated with withdrawal from social interactions. Thus, established interventions for SA should be adjusted when targeting loneliness.SIGNIFICANCE STATEMENT Loneliness can cause serious health problems. Adapting well-established cognitive-behavioral therapies targeting social anxiety might be promising to reduce chronic loneliness given a close link between both constructs. However, a better understanding of behavioral and neurobiological factors associated with loneliness is needed to identify which specific mechanisms of social anxiety are shared by lonely individuals. We found that lonely individuals show a consistently distinct pattern of behavioral and neural responsiveness to social decision-making and social feedback compared with previous findings for social anxiety. Our results indicate that loneliness is associated with a biased emotional reactivity to negative events rather than social avoidance. Our findings thus emphasize the distinctiveness of loneliness from social anxiety and the need for adjusted psychotherapeutic protocols.

Differential contribution of between and within-brain coupling to movement synchronization.

A fundamental characteristic of the human brain that supports behavior is its capacity to create connections between brain regions. A promising approach holds that during social behavior, brain regions not only create connections with other brain regions within a brain, but also coordinate their activity with other brain regions of an interaction partner. Here we ask whether between-brain and within-brain coupling contribute differentially to movement synchronization. We focused on coupling between the inferior frontal gyrus (IFG), a brain region associated with the observation-execution system, and the dorsomedial prefrontal cortex (dmPFC), a region associated with error-monitoring and prediction. Participants, randomly divided into dyads, were simultaneously scanned with functional near infra-red spectroscopy (fNIRS) while performing an open-ended 3D hand movement task consisting of three conditions: back-to-back movement, free movement, or intentional synchronization. Results show that behavioral synchrony was higher in the intentional synchrony compared with the back-to-back and free movement conditions. Between-brain coupling in the IFG and dmPFC was evident in the free movement and intentional synchrony conditions but not in the back-to-back condition. Importantly, between-brain coupling was found to positively predict intentional synchrony, while within-brain coupling was found to predict synchronization during free movement. These results indicate that during intentional synchronization, brain organization changes such that between-brain networks, but not within-brain connections, contribute to successful communication, pointing to shift from a within-brain feedback loop to a two-brains feedback loop.

Altered activation in the action observation system during synchronization in high loneliness individuals.

Lonely people tend to evaluate social exchanges negatively and to display difficulties in interactions. Interpersonal synchronization is crucial for achieving positive interactions, promoting affinity, closeness, and satisfaction. However, little is known about lonely individuals' ability to synchronize and about their brain activity while synchronizing. Following the screening of 303 participants, we recruited 32 low and 32 high loneliness participants. They were scanned while engaged in movement synchronization, using a novel dyadic interaction paradigm. Results showed that high loneliness individuals exhibited a reduced ability to adapt their movement to their partner's movement. Intriguingly, during movement adaptation periods, high loneliness individuals showed increased activation in the action observation (AO) system, specifically in the inferior frontal gyrus and the inferior parietal lobule. They did not show increased activation in the dorsomedial prefrontal cortex, which in the context of synchronization was suggested to be related to gap-monitoring. Based on these findings, we propose a model according to which lonely people may require stronger activation of their AO system for alignment, to compensate for some deficiency in their synchronization ability. Despite this hyperactivation, they still suffer from reduced synchronization capacity. Consequently, synchronization may be a relevant intervention area for the amelioration of loneliness.

Brain-to-brain coupling during handholding is associated with pain reduction.

The mechanisms underlying analgesia related to social touch are not clear. While recent research highlights the role of the empathy of the observer to pain relief in the target, the contribution of social interaction to analgesia is unknown. The current study examines brain-to-brain coupling during pain with interpersonal touch and tests the involvement of interbrain synchrony in pain alleviation. Romantic partners were assigned the roles of target (pain receiver) and observer (pain observer) under pain-no-pain and touch-no-touch conditions concurrent with EEG recording. Brain-to-brain coupling in alpha-mu band (8-12 Hz) was estimated by a three-step multilevel analysis procedure based on running window circular correlation coefficient and post hoc power of the findings was calculated using simulations. Our findings indicate that hand-holding during pain administration increases brain-to-brain coupling in a network that mainly involves the central regions of the pain target and the right hemisphere of the pain observer. Moreover, brain-to-brain coupling in this network was found to correlate with analgesia magnitude and observer's empathic accuracy. These findings indicate that brain-to-brain coupling may be involved in touch-related analgesia.

Oxytocin increases the social salience of the outgroup in potential threat contexts.

A growing body of literature suggests that OT administration may affect not only prosocial outcomes, but also regulate adversarial responses in the context of intergroup relations. However, recent reports have challenged the view of a fixed role of OT in enhancing ingroup favoritism and outgroup derogation. Studying the potential effects of OT in modulating threat perception in a context characterized by racial miscegenation (Brazil) may thus afford additional clarification on the matter. In a double-blind, placebo-controlled study, White Brazilian participants completed a first-person shooter task to assess their responses towards potential threat from racial ingroup (White) or outgroup (Black) members. OT administration enhanced the social salience of the outgroup, by both increasing the rate at which participants refrained from shooting unarmed Black targets to levels similar to White targets, and by further increasing the rate of correct decisions to shoot armed Black targets (versus White armed targets). In summary, our results indicate that a single dose of OT may promote accurate behavioral responses to potential threat from members of a racial outgroup, thus offering support to the social salience hypothesis.

Women's Body Odor during Ovulation Improves Social Perception in Single Men.

Previous research has shown that men's mating motivation may increase following exposure to women's body odor during ovulation. In the current study, we examined whether exposure to women's fertility odor cues influences social perception among men, while focusing on the role of men's relationship status in moderating this reaction. We collected body odor samples from 43 women during ovulation and during the luteal phase and exposed 85 men to these odor samples while they performed an emotion recognition task and an interpersonal perception task. Single men were better at recognizing emotional facial expressions following exposure to odor cues of high fertility as compared with odor cues of low fertility. No such effect was identified in pair-bonded men. In support of this finding, single men became more accurate on the interpersonal perception task following exposure to odor cues of high fertility, while pair-bonded men became less accurate after such exposure. Collectively, the results suggest that exposure to women's fertility odor cues improves social perception among single men, while it impairs such perception among pair-bonded men. We suggest that these effects may result from increased mating motivation following exposure to odor cues of fertility, which in turn encourages accurate social perception among single men while promoting an avoidant attitude toward social stimuli among pair-bonded men.

A Time-Varying Measure of Dyadic Synchrony for Three-Dimensional Motion.

We propose a novel approach to the analysis of synchronized three-dimensional motion in dyads. Motion recorded at high time resolution, as with a gaming device, is preprocessed in each of the three spatial dimensions by spline smoothing. Synchrony is then defined, at each time point, as the cosine between the two individuals' estimated velocity vectors. The approach is extended to allow a time lag, allowing for the analysis of leader-follower dynamics. Mean square cosine over the time range is proposed as a scalar summary of dyadic synchrony, and this measure is found to be positively associated with cognitive empathy.

The neural underpinnings of cross-cultural differences in creativity.

Whereas Western individualistic cultures emphasize uniqueness, collectivistic East-Asian cultures discourage it. Here we examined whether cross-cultural differences in creativity as measured by a task of divergent thinking (DT) are explained by enhanced activity in brain regions that mediate inhibitory control (e.g., the left inferior frontal gyrus [L-IFG]). We therefore predicted that the L-IFG would be "hyperactive" among individuals from East-Asian cultures compared to Western ones. In Study 1, Israeli and South Korean participants were compared on a classic DT task (AUT; "Alternate uses: Manual of instructions and interpretation"). Israelis generated more original ideas compared to South Koreans. In Study 2, Israeli participants and South Korean participants currently living in Israel were scanned while performing the AUT. In line with previous studies, the results indicate that generation of original ideas across cultures is associated with activation of the posterior cingulate cortex (PCC), which is part of the default mode network (DMN). As hypothesized, South Koreans showed enhanced activation of the L-IFG compared to Israelis. This enhanced activation was associated with lower originality scores. The cultural dimension of traditionalism, being higher in the South Korean sample than in the Israeli Sample, was related to enhance L-IFG activity, further supporting our hypothesis regarding cultural influences on inhibitory control. Furthermore, functional connectivity analysis indicated that activation of the L-IFG was positively coupled with PCC activity among Israelis and with preSMA activity among South Koreans. The results suggest that cross-cultural differences in creativity might be explained by variations in inhibitory control.

Androstadienone, a Chemosignal Found in Human Sweat, Increases Individualistic Behavior and Decreases Cooperative Responses in Men.

A growing body of evidence suggests that humans can communicate socially relevant information, such as aggression, dominance, and readiness for competition, through chemosensory signals. Androstadienone (androsta-4,16,-dien-3-one), a testosterone-derived compound found in men's axillary sweat, is a main candidate for a human pheromone that may convey such information. The current study aimed to investigate whether androstadienone serves as a chemosignaling threat cue to men, thus triggering avoidance behavior during competitive interaction with another man. In a double-blind, placebo-controlled, within-subject study design, 30 healthy, normosmic, heterosexual male participants completed the social orientation paradigm (SOP), a monetary game played against a fictitious partner that allows 3 types of responses to be measured in the context of provocation: an aggressive response, an individualistic withdrawal response, and a cooperative response. Participants completed the SOP task twice, once under exposure to androstadienone and once under exposure to a control solution. The results indicate that androstadienone increased individualistic responses while it decreased cooperative responses. These findings support the role of androstadienone as a threatening signal of dominance that elicits behavioral avoidance and social withdrawal tendencies, possibly as a submissive response.

The impact of empathy and reappraisal on emotional intensity recognition.

Empathy represents a fundamental ability that allows for the creation and cultivation of social bonds. As part of the empathic process, individuals use their own emotional state to interpret the content and intensity of other people's emotions. Therefore, the current study was designed to test two hypotheses: (1) empathy for the pain of another will result in biased emotional intensity judgment; and (2) changing one's emotion via emotion regulation will modulate these biased judgments. To test these hypotheses, in experiment one we used a modified version of a well-known task that triggers an empathic reaction We found that empathy resulted in biased emotional intensity judgment. To the best of our knowledge, this is the first demonstration of a bias in the recognition of emotional facial expressions as a function of empathy for pain. In experiment two, we replicated these findings in an independent sample, and further found that this biased emotional intensity judgment can be moderated via reappraisal. Taken together, our findings suggest that the novel task used here can be employed to further explore the relation between emotion regulation and empathy.

The role of empathy in the neural responses to observed human social touch.

One of the ways in which individuals convey feelings and thoughts to one another is through touch. Although the neural responses to felt and observed tactile stimuli between an inanimate object and a part of the human body have been vastly explored, the neural responses to observed human interaction involving touch are not well understood. Considering that the observation of social touch involves vicarious sharing of emotions, we hypothesized that levels of empathic traits modulate the neural responses to observed touch and focused on the attenuation in the mu\alpha rhythm (8-13Hz), a neural marker that has been related to sensorimotor resonance. Fifty-four participants observed photos depicting social touch, nonsocial touch, or no touch while their electroencephalography (EEG) activity was recorded. Results showed that interindividual differences in levels of empathic traits modulated both behavioral and electrophysiological responses to human social touch, such that highly empathic participants evaluated human social touch as inducing more pleasant emotions and exhibited greater mu suppression upon observation of human social touch compared to less empathic participants. Specifically, both the behavioral and the electrophysiological responses to observed social touch were predicted by levels of personal distress, a measure of emotional contagion. These findings indicate that the behavioral and electrophysiological responses to observed social touch are modulated by levels of empathy.

Generating original ideas: The neural underpinning of originality.

One of the key aspects of creativity is the ability to produce original ideas. Originality is defined in terms of the novelty and rarity of an idea and is measured by the infrequency of the idea compared to other ideas. In the current study we focused on divergent thinking (DT) - the ability to produce many alternate ideas - and assessed the neural pathways associated with originality. Considering that generation of original ideas involves both the ability to generate new associations and the ability to overcome automatic common responses, we hypothesized that originality would be associated with activations in regions related to associative thinking, including areas of the default mode network (DMN) such as medial prefrontal areas, as well as with areas involved in cognitive control and inhibition. Thirty participants were scanned while performing a DT task that required the generation of original uses for common objects. The results indicate that the ability to produce original ideas is mediated by activity in several regions that are part of the DMN including the medial prefrontal cortex (mPFC) and the posterior cingulate cortex (PCC). Furthermore, individuals who are more original exhibited enhanced activation in the ventral anterior cingulate cortex (vACC), which was also positively coupled with activity in the left occipital-temporal area. These results are in line with the dual model of creativity, according to which original ideas are a product of the interaction between a system that generates ideas and a control system that evaluates these ideas.

Away from the herd: loneliness as a dysfunction of social alignment.

The tendency of all humans to experience loneliness at some point in their lives implies that it serves an adaptive function. Building on biological theories of herding in animals, according to which collective movement emerges from local interactions that are based on principles of attraction, repulsion and alignment, we propose an approach that synthesizes these principles with theories of loneliness in humans. We present here the 'herding model of loneliness' that extends these principles into the psychological domain. We hold that these principles serve as basic building blocks of human interactions and propose that distorted attraction and repulsion tendencies may lead to inability to align properly with others, which may be a core component in loneliness emergence and perpetuation. We describe a neural model of herding in humans and suggest that loneliness may be associated with altered interactions between the gap/error detection, reward signaling, threat and observation-execution systems. The proposed model offers a framework to predict the behavior of lonely individuals and thus may inform intervention designs for reducing loneliness intensity.

Post-interaction neuroplasticity of inter-brain networks underlies the development of social relationship.

Inter-brain coupling has been increasingly recognized for its role in supporting connectedness during social communication. Here we investigate whether inter-brain coupling is plastic and persists beyond the offset of social interaction, facilitating the emergence of social closeness. Dyads were concurrently scanned using functional near infrared spectroscopy (fNIRS) while engaging in a task that involved movement synchronization. To assess post-interaction neuroplasticity, participants performed a baseline condition with no interaction before and after the interaction. The results reveal heightened inter-brain coupling in neural networks comprising the inferior frontal gyrus (IFG) and dorsomedial prefrontal cortex in the post-task compared to the pre-task baseline. Critically, the right IFG emerged as a highly connected hub, with post-task inter-brain coupling in this region predicting the levels of motivation to connect socially. We suggest that post-interactions inter-brain coupling may reflect consolidation of socially related cues, underscoring the role of inter-brain plasticity in fundamental aspects of relationship development.

When two become one: the role of oxytocin in interpersonal coordination and cooperation.

Cooperation involves intentional coordinated acts performed to achieve potentially positive outcomes. Here we present a novel explanatory model of cooperation, which focuses on the role of the oxytocinergic system in promoting interpersonal coordination and synchrony. Cooperation was assessed using a novel computerized drawing task that may be performed individually or cooperatively by two participants who coordinate their actions. Using a within-subject crossover design, 42 participants performed the task alone and with a partner following the administration of placebo and oxytocin 1 week apart. The data indicate that following placebo administration, participants performed better alone than in pairs. Yet, the administration of oxytocin improved paired performance up to the level of individual performance. This effect depended on the personality traits of cooperativeness or competitiveness. It is concluded that oxytocin may play a key role in enhancing social synchrony and coordination of behaviors required for cooperation.

Don't stand so close to me: a behavioral and ERP study of preferred interpersonal distance.

The space between people, or interpersonal distance, creates and defines the dynamics of social interactions. Given that invasion of one's interpersonal space may trigger threat and anxiety, a critical question is if high vulnerability to social anxiety (SA) is associated with avoidance and attentional biases when anticipating invasion to one's interpersonal space. Therefore, the current study sought to examine the behavioral mechanisms, time course and neural correlates underlying the threat of interpersonal distance invasion with a focus on different SA levels, using both a behavioral and an ERP experiment. Preferred interpersonal distance was assessed using a paradigm that involves responding to different virtual protagonists (friend or stranger) approaching the participant by indicating where one would like the protagonist to stop. In addition, participants' level of social anxiety was measured. The behavioral experiment indicated that levels of SA predicted one's preferred interpersonal distance such that higher SA individuals preferred further distance from a stranger. At the neural level, across groups, early (N1) but not late (LPP) differences were found between stranger and friend conditions. Importantly, SA individuals were characterized by attenuated early ERP responses, suggesting less attentional resources allocated to social stimuli. The results suggest that high SA individuals feel discomfort earlier than others in social engagement, which may lead them to stand further away, thus creating less communicative social interactions.

Sensitivity to fairness and intentions of others in the ultimatum game in patients with ventromedial prefontal lesions.

This study aimed to examine the relationship between perspective-taking and impaired decision-making in patients with ventromedial prefrontal (VM) lesions, using the Ultimatum Game (UG). In the UG, two players split a sum of money and one player proposes a division while the other can accept or reject this. Eight patients with VM damage and 18 healthy controls participated as responders in a modified version of the UG, in which identical offers can generate different rejection rates depending on the other offers available to the proposer. Participants had to either accept or reject offers of 2:8 NIS (2NIS for them and 8 NIS for the proposer), which were paired with one of four different possible offers (5:5, 4:6, 2:8, 8:2). Results indicate that the controls more often rejected offers of 2:8 when the alternative was 4:6 (a greedy alternative) than when the alternative was 5:5 (fair alternative), whereas the VM patients showed the opposite pattern of decision-making. Additionally, the overall rejection rates were higher in patients as compared to controls. Furthermore, scores on a perspective-taking scale were negatively correlated with rejection rates in the patient group, suggesting that perspective-taking deficits may account for impaired decision-making in VM patients.

Brains that Fire Together Wire Together: Interbrain Plasticity Underlies Learning in Social Interactions.

Social interactions are powerful determinants of learning. Yet the field of neuroplasticity is deeply rooted in probing changes occurring in synapses, brain structures, and networks within an individual brain. Here I synthesize disparate findings on network neuroplasticity and mechanisms of social interactions to propose a new approach for understanding interaction-based learning that focuses on the dynamics of interbrain coupling. I argue that the facilitation effect of social interactions on learning may be explained by interbrain plasticity, defined here as the short- and long-term experience-dependent changes in interbrain coupling. The interbrain plasticity approach may radically change our understanding of how we learn in social interactions.

Adaptive Empathy: A Model for Learning Empathic Responses in Response to Feedback.

Empathy is usually deployed in social interactions. Nevertheless, common measures and examinations of empathy study this construct in isolation from the person in distress. In this article we seek to extend the field of examination to include both empathizer and target to determine whether and how empathic responses are affected by feedback and learned through interaction. Building on computational approaches in feedback-based adaptations (e.g., no feedback, model-free and model-based learning), we propose a framework for understanding how empathic responses are learned on the basis of feedback. In this framework, adaptive empathy, defined as the ability to adapt one's empathic responses, is a central aspect of empathic skills and can provide a new dimension to the evaluation and investigation of empathy. By extending existing neural models of empathy, we suggest that adaptive empathy may be mediated by interactions between the neural circuits associated with valuation, shared distress, observation-execution, and mentalizing. Finally, we propose that adaptive empathy should be considered a prominent facet of empathic capabilities with the potential to explain empathic behavior in health and psychopathology.

The benefits of learning movement sequences in social interactions.

Although we frequently acquire knowledge and skills through social interactions, the focus of most research on learning is on individual learning. Here we characterize Interaction Based Learning (IBL), which represents the acquisition of knowledge or skill through social interactions, and compare it to Observational Learning (OL)-learning by observation. To that end, we designed a movement synchronization paradigm whereby participants learned Tai-Chi inspired movement sequences from trained teachers in two separated sessions. We used a motion capture system to track the movement of 40 dyads comprised of a teacher and learner, who were randomly divided into OL or IBL groups, and calculated time-varying synchrony of three-dimensional movement velocity. While in the IBL group both the learner and the teacher could see each other through a transparent glass, in the OL group dyads interacted through a one-way mirror, such that the learners observed the teacher, but the teacher could not see the learners. Results show that although the number of movements recalled was not different between groups, we found improved movement smoothness in the IBL compared to the OL group, indicating movement acquisition was better in the IBL group. In addition, we found that motor synchronization levels in dyads improved over time, indicating that movement synchronization can be learned and retained. In the first session, the IBL group, but not the OL group, showed a significant improvement in synchronization. This suggests that dyadic interaction is important for learning movement sequences, and that bidirectional communication of signals and mutual feedback are essential for the consolidation of motor learning.