An oxytocin-induced facilitation of neural and emotional responses to social touch correlates inversely with autism traits

Abstract

Social communication through touch and mutual grooming can convey highly salient socio-emotional signals and has been shown to involve the neuropeptide oxytocin (OXT) in several species. Less is known about the modulatory influence of OXT on the neural and emotional responses to human interpersonal touch. The present randomized placebo (PLC)-controlled within-subject pharmaco-functional magnetic resonance imaging (fMRI) study was designed to test the hypothesis that a single intranasal dose of synthetic OXT (24 IU) would facilitate both neural and emotional responses to interpersonal touch in a context- (female vs male touch) and trait- (autistic trait load) specific manner. Specifically, the experimental rationale was to manipulate the reward value of interpersonal touch independent of the intensity and type of actual cutaneous stimulation administered. Thus, 40 heterosexual males believed that they were touched by either a man or a woman, although in fact an identical pattern of touch was always given by the same female experimenter blind to condition type. Our results show that OXT increased the perceived pleasantness of female, but not male touch, and associated neural responses in insula, precuneus, orbitofrontal, and pregenual anterior cingulate cortex. Moreover, the behavioral and neural effects of OXT were negatively correlated with autistic-like traits. Taken together, this is the first study to show that the perceived hedonic value of human heterosexual interpersonal touch is facilitated by OXT in men, but that its behavioral and neural effects in this context are blunted in individuals with autistic traits.

Figure 1

OXT effects on the pleasantness of touch. Intranasal administration of OXT specifically increased the pleasantness of female touch (a) and had no effect on ratings of male touch or a control condition where the female was at the same spatial distance to the subject but without any tactile contact. The behavioral OXT effect (OXT minus PLC) on female touch was more pronounced in subjects with a low autism-spectrum quotient (b). Error bars indicate the standard error of the mean (SEM). OXT, oxytocin; PLC, placebo. **P<0.01.

Figure 2

OXT effects on female touch. OXT specifically enhanced neural responses to female touch in insula cortex (a), precuneus (b), orbitofrontal cortex (c), and pregenual anterior cingulate cortex (d). The shaded area represents the standard error of the mean (SEM) and the gray area indicates the duration of touch. L, left; OFC, orbitofrontal cortex; OXT, oxytocin; pACC, pregenual anterior cingulate cortex; PLC, placebo; R, right.

Figure 3

Autistic traits differentially moderate the neural response to female and male touch. Under oxytocin, neural responses to touch in the orbitofrontal cortex are negatively correlated with autistic traits in the female touch condition (a) and positively correlated in the male touch condition (b). AQ, autism-spectrum quotient; L, left; OFC, orbitofrontal cortex; OXT, oxytocin; PLC, placebo; R, right.