Touching upon affiliation: On the roles of the opioid and oxytocin systems in human social-emotional behavior

Abstract

Humans are fundamentally social animals. Since they depend on each other for survival and well-being, their social skills are essential to facilitate communication, conflict resolution and formation and maintenance of social bonds. The superb social abilities bring sensitivities: the experience of being excluded from a group of friends or being rejected from a partner is remarkably painful, up to a physical level. In the long-term, social isolation and perceived loneliness are known risk factors for physical and mental health problems, as they activate stress related psychological and neurobiological mechanisms. The aim of this thesis is to systematically investigate aspects of social-emotional behavior that support social affiliation and protect from the aversive consequences of experiencing social rejection and isolation. Crucially, the contributing role of oxytocin and opioid systems to these behaviors will be discussed. The thesis starts with a review and theoretical perspective on the role of the endogenous mu-opioid receptor system in social-emotional behavior. I propose a ‘Mu-opioid feedback model of social behavior’ which suggests that the mu-opioid system regulates affiliative or protective responses to social stimuli through its key function of attributing hedonic value to positive and negative social stimuli, with long-term consequences for social behavior and mental health. In the following three experimental chapters basic, automatic-, as well as more complex, higher-order processes that modulate affiliative motivation are discussed. The first experimental chapter shows that blocking the mu-opioid system pharmacologically with naltrexone modulates the imitation of emotional facial expressions, an automatic behavioral marker of social affiliation. The results therewith provide evidence that the mu-opioid system regulates underlying behavioral responses to affective cues important for affiliation. The next experimental chapter discusses the effects of oxytocin on neural sensitivity to visual signals of reward and distress from children. The neuroimaging results indicate that the effects of oxytocin differ depending on the experience of emotional neglect during childhood. Oxytocin administration results in increased activity in areas involved in emotion processing (amygdala and hippocampus) and decreased activity related in areas of emotion regulation (prefrontal cortex), specifically in individuals who experienced childhood emotional neglect. Hence, oxytocin adjusts the neural activation of individuals who experienced emotional neglect to the one of individuals who experienced no emotional neglect. Finally, the last experimental chapter contributes to literature demonstrating the beneficial effects of social touch as a stress buffer. Using eye-tracking to measure gaze behavior as an indicator of socially dominant vs. anxious behavior, the results show that social touch increases dominant compared to anxious gaze patterns to threatening stimuli. Touch therewith adds to psychological resources useful in challenging situations through increased implicit tendencies to engage in social confrontations.