Oxytocin increases the pleasantness of affective touch and orbitofrontal cortex activity independent of valence

Abstract

Touch plays a crucial role in affiliative behavior and social communication. The neuropeptide oxytocin is released in response to touch and may act to facilitate the rewarding effects of social touch. However, no studies to date have determined whether oxytocin facilitates behavioral or neural responses to non-socially administered affective touch and possible differential effects of touch valence. In a functional MRI experiment using a randomized placebo-controlled, within-subject design in 40 male subjects we investigated the effects of intranasal oxytocin (24IU) on behavioral and neural responses to positive, neutral and negative valence touch administered to the arm via different types of materials at a frequency aimed to optimally stimulate C-fibers. Results showed that oxytocin significantly increased both the perceived pleasantness of touch and activation of the orbitofrontal cortex independent of touch valence. The effects of OT on touch-evoked orbitofrontal activation were also positively associated with basal oxytocin concentrations in blood. Additionally, anterior insula activity and the functional connectivity between the amygdala and right anterior insula were enhanced only in response to negative valence touch. Overall, the present study provides the first evidence that oxytocin may facilitate the rewarding effects of all types of touch, irrespective of valence.

The Effects of Intranasal Oxytocin on Neural and Behavioral Responses to Social Touch in the Form of Massage

“…In line with previous social/affective touch studies (Scheele et al, 2014a;Chen et al, 2020), we found that intranasal OT administration increased ratings of pleasantness for manual massage. However, in contrast to Scheele et al (2014a), but in line with those in our previous study (Li et al, 2019), we found no evidence for any modulatory effect of what sex the subjects thought the masseur was, which may reflect cultural differences as already discussed.…”

“…This was in marked contrast to combined real and imagined machine massage where it produced no significant changes at all at the whole brain level. Not only were neural responses significantly increased in the OFC, AI and ACC, in line with a previous study on Caucasian males touched on their leg by an unseen female (Scheele et al, 2014a) and a study on Chinese males touched on their arm (Chen et al, 2020), but also in a far more extensive network of regions involved in attention, emotion, reward, salience, social cognition, sensorimotor and visual processing.…”

“…They are also similar to those reported in a study on both mothers and fathers prior to skin to skin contact with infants and also using an RIA (Velandia, 2012). Furthermore, they are equivalent to those we have reported previously (Li et al, 2019;Chen et al, 2020) and also from another independent group on Chinese subjects with the more extensively used ENZO ELISA following extraction (Zhang et al, 2016). We cannot, however, entirely rule out the possibility that the antibodies in the assays were also sensitive to some OT fragments although this is a potential issue for all types of OT assays.…”

“…A subsequent study in the context of romantic relationships found similar effects of OT only when subjects thought the touch was applied by their partner and not by an unfamiliar person of the opposite sex (Kreuder et al, 2017). By further excluding social intention and relationship context, a more recent study using well-controlled CT-targeted affective touch with different valences has revealed a general effect of intranasal OT on increasing both the perceived pleasantness of touch and OFC activation independent of touch valence (Chen et al, 2020). Thus, we hypothesized that intranasal administration of OT would enhance the perceived pleasantness of massage, and associated brain reward responses, independent of who administers the massage, since subjects are mainly responding to the hedonic properties of being touched manually independent of the identity of the person administering it.…”

“…Additionally, blood samples were taken to measure basal plasma OT concentrations and autistic traits were measured using the Autism Spectrum Quotient (ASQ - Baron-Cohen et al, 2001) to investigate their respective associations with effects of intranasal OT on individual responses to massage. Based on the demonstrated facilitatory effects of OT on social and affective touch (Scheele et al, 2014a;Chen et al, 2020) and previous findings that manual massage increased OT release (Morhenn et al, 2012;Li et al, 2019), we hypothesized that intranasal OT would significantly increase the perceived pleasantness and corresponding activity in brain regions associated with social touch processing in response to real or imagined massage administered manually but not by machine. Given the negative correlations between OT-induced behavioral and neural effects to touch and autistic traits and the negative correlations between massage-evoked OT concentration changes and autistic traits (Scheele et al, 2014a;Li et al, 2019), we additionally hypothesized that OT-induced responses to massage would be associated with basal OT concentrations in the blood and trait autism.…”