Humans belong to a minority of mammalian species that exhibit monogamous pair-bonds, thereby enabling biparental care of offspring. The high reward value of interpersonal closeness and touch in couples is a key proximate mechanism facilitating the maintenance of enduring romantic bonds. However, surprisingly, the neurobiological underpinnings mediating the unique experience of a romantic partner's touch remain unknown. In this randomized placebo (PLC)-controlled, between-group, pharmacofunctional magnetic resonance imaging (fMRI) study involving 192 healthy volunteers (96 heterosexual couples), we intranasally administered 24 IU of the hypothalamic peptide oxytocin (OXT) to either the man or the woman. Subsequently, we scanned the subjects while they assumed that they were being touched by their romantic partners or by an unfamiliar person of the opposite sex, although in reality an identical pattern of touch was always given by the same experimenter. Our results show that intranasal OXT compared to PLC selectively enhanced the subjective pleasantness of the partner's touch. Importantly, intranasal OXT selectively increased responses to partner touch in the nucleus accumbens (NAcc) and anterior cingulate cortex. Under OXT, NAcc activations to partner touch positively correlated with the subjects' evaluation of their relationship quality. Collectively, our results suggest that OXT may contribute to the maintenance of monogamous relationships in humans by concomitantly increasing the reward value of partner touch and diminishing the hedonic quality of stranger touch. Hum Brain Mapp 38:4525-4534, 2017. © 2017 Wiley Periodicals, Inc.

Social support plays a vital role in physical and mental well-being. The neuropeptide hormone oxytocin (OXT) has been implicated in modulating pair-bonding and affiliative behaviors, but whether OXT contributes to the analgesic effects of a romantic partner's touch remains elusive. In the present randomized placebo-controlled, between-group, functional magnetic resonance imaging study involving 194 healthy volunteers (97 heterosexual couples), we tested the effects of intranasal OXT (24 IU) on handholding as a common mode of expressing emotional support in romantic couples. We scanned the subjects while brief electric shocks were administered. The subjects assumed that they received social support from either their romantic partner or an unfamiliar person. Unbeknown to the subject, in the partner and stranger support conditions, the same male experimenter always held the subject's left hand. Partner support was most effective in reducing the unpleasantness of electric shocks, and OXT further attenuated the unpleasantness across conditions. On the neural level, OXT significantly augmented the beneficial effects of partner support, as evidenced by a stronger decrease of neural responses to shocks in the anterior insula (AI), a stronger activity increase in the middle frontal gyrus (MFG), and a strengthened functional coupling between the AI and MFG. Our results support the notion that OXT specifically modulates the beneficial effects of social support in romantic couples by concomitantly reducing pain-associated activity and increasing activity linked to cognitive control and pain inhibition. We hypothesize that impaired OXT signaling may contribute to the experience of a lack of partner support.