Impairment in reading negative social cues extends beyond the face in autism.

Nonverbal expressions are essential to regulating social communication and interaction. Impaired emotion recognition from facial expressions has been linked to various psychiatric conditions characterized by severe social deficits such as autism. As body expressions as an additional source of social-emotional information have attracted little research attention, little is known about whether emotion recognition impairments are specific to faces, or extend to body expressions. This study explored and compared emotion recognition from face versus body expressions in autism spectrum disorder. We compared 30 men with autism spectrum disorder to 30 male age- and IQ-matched control participants in their ability to recognize angry, happy, and neutral expressions from dynamic face and body expressions. Participants with autism spectrum disorder showed impaired recognition of angry expressions from both faces and bodies, while there were no group differences in recognizing happy and neutral expressions. In autism spectrum disorder, recognizing angry face expressions was inversely predicted by gaze avoidance, while recognizing angry body expressions was inversely predicted by impairments in social interaction and autistic traits. These findings suggest that distinct mechanisms may underlie the impaired emotion recognition from face and body expressions in autism spectrum disorder, respectively. Overall, our study demonstrates that emotion-specific recognition difficulties in autism spectrum disorder are not limited to face expressions but extend to emotional body expressions.

EmBody/EmFace as a new open tool to assess emotion recognition from body and face expressions.

Nonverbal expressions contribute substantially to social interaction by providing information on another person's intentions and feelings. While emotion recognition from dynamic facial expressions has been widely studied, dynamic body expressions and the interplay of emotion recognition from facial and body expressions have attracted less attention, as suitable diagnostic tools are scarce. Here, we provide validation data on a new open source paradigm enabling the assessment of emotion recognition from both 3D-animated emotional body expressions (Task 1: EmBody) and emotionally corresponding dynamic faces (Task 2: EmFace). Both tasks use visually standardized items depicting three emotional states (angry, happy, neutral), and can be used alone or together. We here demonstrate successful psychometric matching of the EmBody/EmFace items in a sample of 217 healthy subjects with excellent retest reliability and validity (correlations with the Reading-the-Mind-in-the-Eyes-Test and Autism-Spectrum Quotient, no correlations with intelligence, and given factorial validity). Taken together, the EmBody/EmFace is a novel, effective (< 5 min per task), highly standardized and reliably precise tool to sensitively assess and compare emotion recognition from body and face stimuli. The EmBody/EmFace has a wide range of potential applications in affective, cognitive and social neuroscience, and in clinical research studying face- and body-specific emotion recognition in patient populations suffering from social interaction deficits such as autism, schizophrenia, or social anxiety.

Kinetics of oxytocin effects on amygdala and striatal reactivity vary between women and men.

Accumulating evidence suggests that intranasal oxytocin (OXT; 24 IU) reduces amygdala responses to fear-related stimuli in men, while exerting inverse effects in women. However, OXT enhances activity of the brain reward system in both sexes. Importantly, a crucial and still open question is whether there are sex-specific dose-response relationships for the amygdala and striatal regions. To address this question, a total of 90 healthy women participated in a double-blind, placebo-controlled crossover functional magnetic resonance imaging (fMRI) study and the results were compared with our previous findings from men. Participants were randomly assigned to three doses of OXT (6 IU, 12 IU, and 24 IU) and completed an emotional face recognition task including fearful and happy faces of varying emotional intensities. Across doses, OXT enhanced amygdala reactivity to low fearful faces compared to placebo and increased responses to happy faces in the dorsal striatum in women. While treatment effects on amygdala reactivity were evident at each given dose, the OXT effect on striatal responses to social stimuli was more pronounced with higher doses, but this dose-dependent effect did not survive correction for multiple comparisons. Importantly, OXT effects on amygdala and striatal activation significantly differed between sexes and striatal baseline sexual-dimorphic response patterns were diminished after administration of OXT. Our findings suggest that OXT increases the salience of social signals by strengthening the sensitivity for these signals in the amygdala and in the striatum in women, while OXT may primarily induce anxiolysis by reducing amygdala responses in men.

Effects of intranasal oxytocin administration on empathy and approach motivation in women with borderline personality disorder: a randomized controlled trial.

Borderline personality disorder (BPD) is characterized by severe interpersonal dysfunction with problems in social cognition, empathy and social approach. Although the neuropeptide oxytocin is known to regulate complex social cognition and behavior in healthy individuals and clinical populations, there is still a lack of evidence for a potential beneficial effect of oxytocin administration on social cognition and social approach in BPD. Fifty-one women with BPD and 51 matched healthy controls were randomized to a double-blind, placebo-controlled, between-subject experimental trial. We administered a single dose of 24 IU oxytocin or placebo intranasally prior to a standardized task measuring affective and cognitive empathy and approach motivation. All participants were free of hormonal contraception and tested in the mid-luteal phase of their menstrual cycle. In the placebo condition, patients with BPD showed reduced cognitive and affective empathy, and less approach behavior motivation than healthy controls. Intranasal oxytocin significantly increased affective empathy and approach motivation in both BPD patients and healthy controls compared to placebo. More importantly, oxytocin administration led to similar scores between BPD and healthy controls. These findings provide the first evidence for a beneficial effect of oxytocin on deficits in affective empathy and approach motivation of BPD. Our results indicate a beneficial effect of a single dose of oxytocin on affective empathy and approach motivation in women with BPD adapting their level of social functioning to healthy controls. Future clinical trials will need to investigate the long-term effects and effectiveness of oxytocin as an add-on treatment for social impairments in BPD.

A Protective Mechanism against Illusory Perceptions Is Amygdala-Dependent.

Most people have a clear sense of body ownership, preserving them from physical harm. However, perceptual body illusions - famously the rubber hand illusion (RHI) - can be elicited experimentally in healthy individuals. We hypothesize that the amygdala, a core component of neural circuits of threat processing, is involved in protective mechanisms against disturbed body perceptions. To test this hypothesis, we started by investigating two monozygotic human twin sisters with focal bilateral amygdala damage due to Urbach-Wiethe disease. Relative to 20 healthy women, the twins exhibited, on two occasions 1 year apart, augmented RHI responses in form of faster illusion onset and increased vividness ratings. Following up on these findings, we conducted a volumetric brain morphometry study involving an independent, gender-mixed sample of 57 healthy human volunteers (36 female, 21 male). Our results revealed a positive correlation between amygdala volume and RHI onset, i.e., the smaller the amygdala, the less time it took the RHI to emerge. This raised the question of whether a similar phenotype would result from experimental amygdala inhibition. To dampen amygdala reactivity, we intranasally administered the peptide hormone oxytocin to the same 57 individuals in a randomized trial before conducting the RHI. Compared with placebo, oxytocin treatment yielded enhanced RHI responses, again evident in accelerated illusion onset and increased vividness ratings. Together, the present series of experiments provides converging evidence for the amygdala's unprecedented role in reducing susceptibility to the RHI, thus protecting the organism from the potentially fatal threats of a distorted bodily self.SIGNIFICANCE STATEMENT Compelling evidence indicates that the amygdala is of vital importance for danger detection and fear processing. However, lethal threats can arise not only from menacing external stimuli but also from distortions in bodily self-perception. Intriguingly, the amygdala's modulatory role in such illusory body perceptions is still elusive. To probe the amygdala's involvement in illusory body experiences, we conducted a multi-methodological series of experiments in a rare human amygdala lesion model, complemented by a morphological and pharmaco-modulatory experiment in healthy volunteers. Our findings convergently suggest that the amygdala's integrity is indispensable for maintaining an unbiased, precise perception of our bodily self. Hence, the amygdala might shield us against distortions in self-perception and the resultant loss of behavioral control of our organism.

Oxytocin reduces a chemosensory-induced stress bias in social perception.

Social transmission of fear is not restricted to visual or auditory cues, but extends to the phylogenetically more ancient olfactory domain. Anxious individuals exhibit heightened sensitivity towards chemosensory stress signals in sweat; however, it is still unknown whether endogenous neuromodulators such as the peptide hormone oxytocin (OXT) influence the chemosensory communication of stress. Here, we investigated whether OXT selectively diminishes behavioral and neural responses to social chemosensory stress cues utilizing a randomized, double-blind, placebo (PLC)-controlled, within-subject functional MRI study design. Axillary sweat was obtained from 30 healthy male donors undergoing the Trier Social Stress Test (stress) and bicycle ergometer training (sport). Subsequently, 58 healthy participants (30 females) completed a forced-choice emotional face recognition task with stimuli of varying intensities (neutral to fearful) while they were exposed to both sweat stimuli and a non-social control odor following intranasal OXT or PLC administration, respectively. OXT diminished stress-induced recognition accuracy and response time biases towards fear. On the neural level, OXT reduced stress-evoked responses in the amygdala in both sexes, the anterior cingulate cortex (ACC) in females, and the hippocampus in males. Furthermore, OXT reinstated the functional connectivity between the ACC and the fusiform face area that was disrupted by stress odors under PLC. Our findings reveal a new role for OXT signaling in the modulation of chemosensory communication of stress in humans. Mechanistically, this effect appears to be rooted in a downregulation of stress-induced limbic activations and concomitant strengthening of top-down control descending from the ACC to the fusiform face area.

Kinetics and Dose Dependency of Intranasal Oxytocin Effects on Amygdala Reactivity.

BACKGROUND: Current neuroimaging perspectives on a variety of mental disorders emphasize dysfunction of the amygdala. The neuropeptide oxytocin (OXT), a key mediator in the regulation of social cognition and behavior, accumulates in cerebrospinal fluid after intranasal administration in macaques and humans and modulates amygdala reactivity in both species. However, the translation of neuromodulatory OXT effects to novel treatment approaches is hampered by the absence of studies defining the most effective dose and dose-response latency for targeting the amygdala. METHODS: To address this highly relevant issue, a total of 116 healthy men underwent functional magnetic resonance imaging using a randomized, double-blind, placebo-controlled crossover study design. The experimental rationale was to systematically vary dose-test latencies (15-40, 45-70, and 75-100 minutes) and doses of OXT (12, 24, and 48 international units) in order to identify the most robust effects on amygdala reactivity. During functional magnetic resonance imaging, subjects completed an emotional face recognition task including stimuli with varying intensities ranging from low (highly ambiguous) to high (less ambiguous). RESULTS: Our results indicate that the OXT-induced inhibition of amygdala responses to fear was most effective in a time window between 45 and 70 minutes after administration of a dose of 24 international units. Furthermore, the observed effect was most evident in subjects scoring high on measures of autistic-like traits. Behavioral response patterns suggest that OXT specifically reduced an emotional bias in the perception of ambiguous faces. CONCLUSIONS: These findings provide initial evidence of the most effective dose and dose-test interval for future experimental or therapeutic regimens aimed at targeting amygdala functioning using intranasal OXT administration.

Oxytocin facilitates reciprocity in social communication.

Synchrony in social groups may confer significant evolutionary advantages by improving group cohesion and social interaction. However, the neurobiological mechanisms translating social synchrony into refined social information transmission between interacting individuals are still elusive. In two successively conducted experiments involving a total of 306 healthy volunteers, we explored the involvement of the neuropeptide oxytocin (OXT) in reciprocal social interaction. First, we show that synchronous social interactions evoke heightened endogenous OXT release in dyadic partners. In a second step, we examined the consequences of elevated OXT concentrations on emotion transmission by intranasally administering synthetic OXT before recording emotional expressions. Intriguingly, our data demonstrate that the subjects' facial and vocal expressiveness of fear and happiness is enhanced after OXT compared with placebo administration. Collectively, our findings point to a central role of social synchrony in facilitating reciprocal communication between individuals via heightened OXT signaling. Elevated OXT concentrations among synchronized individuals seem to augment the partners' emotional expressiveness, thereby contributing to improved transmission of emotional information in social communication.