Eye-Tracking Reveals a Role of Oxytocin in Attention Allocation Towards Familiar Faces.

Visual attention directed towards the eye-region of a face emerges rapidly, even before conscious awareness, and regulates social interactions in terms of approach versus avoidance. Current perspectives on the neuroendocrine substrates of this behavioral regulation highlight a role of the peptide hormone oxytocin (OXT), but it remains unclear whether the facilitating effects of OXT vary as a function of facial familiarity. Here, a total of 73 healthy participants was enrolled in an eye-tracking experiment specifically designed to test whether intranasal OXT (24 IU) augments gaze duration toward the eye-region across four different face categories: the participants' own face, the face of their romantic partner, the face of a familiar person (close friend) or an unfamiliar person (a stranger). We found that OXT treatment induced a tendency to spend more time looking into the eyes of familiar persons (partner and close friend) as compared to placebo. This effect was not evident in the self and unfamiliar conditions. Independent of treatment, volunteers scoring high on autistic-like traits (AQ-high) spent less time looking at the eyes of all faces except their partner. Collectively, our results show that the OXT system is involved in facilitating an attentional bias towards the eye region of familiar faces, which convey safety and support, especially in anxious contexts. In contrast, autistic-like traits were associated with reduced attention to the eye region of a face regardless of familiarity and OXT-treatment.

Oxytocin and the Neurobiology of Prosocial Behavior.

Humans are an unusually prosocial species, who engage in social behaviors that include altruism-whereby an individual engages in costly or risky acts to improve the welfare of another person-care, and cooperation. Current perspectives on the neurobiology of human prosociality suggest that it is deeply rooted in the neuroendocrine architecture of the social brain and emphasize the modulatory role of the neuropeptide hormone oxytocin. In this review, we provide a conceptual overview of the neurobiology of prosocial behavior with a focus on oxytocin's modulatory role in human prosociality. Specifically, we aim to encourage a better understanding of the peptide's susceptibility to diverse factors that produce heterogeneity in outcomes and the resulting methodological implications for measuring the behavioral effects of oxytocin in humans. After providing an overview of the state-of-the-art research on oxytocin's exogenous use, we elaborate on the peptide's modulatory role in the context of care-based altruism, cooperation, and conflict and discuss its potential for therapeutic interventions in psychiatric disorders characterized by social dysfunction.

Common and dissociable effects of oxytocin and lorazepam on the neurocircuitry of fear.

Benzodiazepines (BZDs) represent the gold standard of anxiolytic pharmacotherapy; however, their clinical benefit is limited by side effects and addictive potential. Consequently, there is an urgent need to develop novel and safe anxiolytics. The peptide hormone oxytocin (OXT) exhibits anxiolytic-like properties in animals and humans, but whether OXT and BZDs share similar effects on the neural circuitry of fear is unclear. Therefore, the rationale of this ultra-high-field functional MRI (fMRI) study was to test OXT against the clinical comparator lorazepam (LZP) with regard to their neuromodulatory effects on local and network responses to fear-related stimuli. One hundred twenty-eight healthy male participants volunteered in this randomized double-blind, placebo-controlled, between-group study. Before scanning using an emotional face-matching paradigm, participants were randomly administered a single dose of OXT (24 IU), LZP (1 mg), or placebo. On the behavioral level, LZP, but not OXT, caused mild sedation, as evidenced by a 19% increase in reaction times. On the neural level, both OXT and LZP inhibited responses to fearful faces vs. neutral faces within the centromedial amygdala (cmA). In contrast, they had different effects on intra-amygdalar connectivity; OXT strengthened the coupling between the cmA and basolateral amygdala, whereas LZP increased the interplay between the cmA and superficial amygdala. Furthermore, OXT, but not LZP, enhanced the coupling between the cmA and the precuneus and dorsomedial prefrontal cortex. These data implicate inhibition of the cmA as a common denominator of anxiolytic action, with only OXT inducing large-scale connectivity changes of potential therapeutic relevance.

Unraveling the role of oxytocin in the motivational structure of conflict.

Current psychological perspectives emphasize "attack" and "defense" as the behavioral mechanisms underlying conflict. Here, we extend this view by highlighting the relevance of pathological altruism and the neuroendocrine pathways associated with hostile behaviors. Specifically, we elucidate the modulatory role of the neuropeptide hormone oxytocin in motivating extraordinary levels of in-group commitment that can promote extreme behaviors and endure conflict with out-groups.

Oxytocin shapes the priorities and neural representations of attitudes and values.

The phylogenetically ancient neuropeptide oxytocin has been linked to a plethora of social behaviors. Here, we argue that the action of oxytocin is not restricted to the downstream level of emotional responses, but substantially alters higher representations of attitudes and values by exerting a distant modulatory influence on cortical areas and their reciprocal interplay with subcortical regions and hormonal systems.

Oxytocin-enforced norm compliance reduces xenophobic outgroup rejection.

Never before have individuals had to adapt to social environments defined by such magnitudes of ethnic diversity and cultural differentiation. However, neurobiological evidence informing about strategies to reduce xenophobic sentiment and foster altruistic cooperation with outsiders is scarce. In a series of experiments settled in the context of the current refugee crisis, we tested the propensity of 183 Caucasian participants to make donations to people in need, half of whom were refugees (outgroup) and half of whom were natives (ingroup). Participants scoring low on xenophobic attitudes exhibited an altruistic preference for the outgroup, which further increased after nasal delivery of the neuropeptide oxytocin. In contrast, participants with higher levels of xenophobia generally failed to exhibit enhanced altruism toward the outgroup. This tendency was only countered by pairing oxytocin with peer-derived altruistic norms, resulting in a 74% increase in refugee-directed donations. Collectively, these findings reveal the underlying sociobiological conditions associated with outgroup-directed altruism by showing that charitable social cues co-occurring with enhanced activity of the oxytocin system reduce the effects of xenophobia by facilitating prosocial behavior toward refugees.

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.

Deciphering the modulatory role of oxytocin in human altruism.

Unlike any other species, humans frequently engage in altruistic behaviors by which they increase another individual's welfare even if this implies personal costs. The psychological motives underlying altruistic behaviors remain diverse, ranging from the ability to reciprocate trust and cooperation to bonding and empathizing with family members or even genetically unrelated others. This article explores the neuroendocrine architecture of altruism by emphasizing the crucial role of the evolutionarily highly conserved peptide hormone oxytocin as a modulator of cooperative behaviors including empathy-driven altruism. However, accumulating evidence suggests that oxytocin does not invariably facilitate cooperation but also produces protective or even defensive-aggressive responses in specific social contexts. In addition, we highlight the relevance of message frames as critical determinants of whether the peptide promotes altruism toward prosocial ends.

A matter of distance-The effect of oxytocin on social discounting is empathy-dependent.

Generosity is an important behavior enriching human society and can be observed across cultures. However, generosity has been shown to be modulated as a function of social distance, also referred to as social discounting. Oxytocin and empathy are other factors that have been shown to play an important role in generous behavior. However, how exactly oxytocin and empathy impact social discounting is yet unknown. Here, we administered oxytocin or placebo in a double-blind design, and measured social discounting behavior. Additionally, individual differences in empathy were assessed. Our results show that the effect of oxytocin on generous behavior is modulated by trait empathy; only for those subjects who received oxytocin there was a positive correlation between individual trait empathy and their generous behavior towards close others.

The Neuropeptide Oxytocin Induces a Social Altruism Bias.

Current psychological concepts of social and ecological responsibility emphasize the relevance of altruism, suggesting that more altruistic individuals are more likely to engage in sustainable behaviors. Emerging evidence indicates a central role of the neuropeptide oxytocin in promoting altruism. Whether this influence extends to ecological responsibility or is limited to the social domain remains unknown. In two independent experiments involving 172 human participants, we addressed this question by exposing subjects to a sustainability-related monetary donation task, with the option to support either socially or ecologically framed charities. We found that oxytocin induced a context-dependent change in altruistic behavior away from pro-environmental toward pro-social donations, while keeping constant the overall proportion of donated money. This pro-social bias transcended to the domain of sustainable consumption. Collectively, our findings demonstrate that altruistic priorities vary as a function of oxytocin system activity, which has implications for the promotion of pro-environmental attitudes and eco-friendly behaviors. SIGNIFICANCE STATEMENT: Individual responses to ecological and social sustainability require a shift in personal priorities away from selfish to more altruistic behaviors. Emerging evidence indicates a central role of the hypothalamic peptide oxytocin in promoting altruism, but whether the influence of oxytocin benefits altruistic decision-making in the context of ecological and social sustainability is unclear. In two independent behavioral experiments involving 172 human subjects, we show that heightened oxytocin system activity induces a social altruism bias at the cost of ecological responsibility. Our results have fundamental implications for policy interventions and business strategies designed to sustain ecological resources by suggesting that a social framing may attract more individuals to engage in pro-environmental and eco-friendly behaviors.

The neuropeptide oxytocin modulates consumer brand relationships.

Each year, companies invest billions of dollars into marketing activities to embellish brands as valuable relationship partners assuming that consumer brand relationships (CBRs) and interpersonal relationships rest upon the same neurobiological underpinnings. Given the crucial role of the neuropeptide oxytocin (OXT) in social bonding, this study tests whether OXT-based mechanisms also determine the bond between consumers and brands. We conducted a randomized, placebo-controlled study involving 101 subjects and analyzed the effect of intranasal OXT on consumers' attribution of relationship qualities to brands, brands paired with human celebrity endorsers, and familiar persons. OXT indeed promoted the attribution of relationship qualities not only in the case of social and semi-social stimuli, but also brands. Intriguingly, for subjects scoring high on autistic-like traits, the effect of OXT was completely reversed, evident in even lower relationship qualities across all stimulus categories. The importance of OXT in a CBR context is further corroborated by a three-fold increase in endogenous release of OXT following exposure to one's favorite brand and positive associations between baseline peripheral OXT concentrations and brand relationship qualities. Collectively, our findings indicate that OXT not only plays a fundamental role in developing interpersonal relationships, but also enables relationship formation with objects such as brands.