How the brain codes intimacy: The neurobiological substrates of romantic touch

Abstract

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.

Keywords: fMRI; fidelity; oxytocin; pair-bonding; touch.

Figure 1

Intranasal oxytocin (OXT) specifically enhanced the pleasantness of partner touch (A; t ₍₉₄₎ = 2.02, P < 0.05). There was no OXT effect on pleasantness ratings of interpersonal touch by an unfamiliar opposite‐sex experimenter or the control condition (Close), in which the experimenter or the partner stood at the same distance but did not touch the participant. Salivary OXT concentrations significantly increased in the placebo (PLC) group following interpersonal touch (B; t ₍₄₇₎ = 4.09, P < 0.01). Baseline salivary OXT concentrations positively correlated within the romantic couples (subjects and their partners) (C; OXT group, r ₍₄₄₎ = 0.43, P < 0.01; PLC group, r ₍₄₄₎ = 0.45, P < 0.01). Error bars indicate the standard error of the mean (SEM). Abbreviations: OXT, oxytocin; PLC, placebo; post, after the touch experiment; pre, before the touch experiment.

Figure 2

Intranasal oxytocin (OXT) significantly increased the response to partner touch relative to stranger touch in the bilateral anterior cingulate cortex (peak MNI coordinates x, y, z: 14, 42, 20; t ₍₈₆₎ = 3.73, P _FWE < 0.05, display threshold P < 0.05 uncorrected; peak MNI coordinates x, y, z: −12, 52, 2; t ₍₈₆₎ = 3.87, P _FWE < 0.05, display threshold P < 0.05 uncorrected). Error bars indicate the standard error of the mean (SEM). Abbreviations: ACC, anterior cingulate cortex; L, left hemisphere; OXT, oxytocin; PLC, placebo; R, right hemisphere.

Figure 3

Intranasal oxytocin (OXT) significantly augmented the response to partner relative to stranger touch in the left nucleus accumbens (NAcc) (peak MNI coordinates x, y, z: −12, 6, −8; t ₍₈₆₎ = 2.69, P _FWE < 0.05, display threshold P < 0.05 uncorrected). Under OXT, the neural response in the left NAcc to partner touch compared to stranger touch was more pronounced in participants with high scores in the Passionate Love Scale (peak MNI coordinates x, y, z: −14, 10, −10; t ₍₄₁₎ = 2.98, P _FWE < 0.05, display threshold P < 0.05 uncorrected). There was no significant association in the placebo group. Error bars indicate the standard error of the mean (SEM). Abbreviations: L, left hemisphere; NAcc, nucleus accumbens; OXT, oxytocin; PLC, placebo; R, right hemisphere.