Exploring the Potential of Oxytocin for Enhancing Interpersonal Motor Resonance upon Direct Eye Gaze: A Transcranial Magnetic Stimulation Study

Background: Among different social cues from the environment, the eyes constitute a very salient source for initiating social interaction or communication. Interestingly, previous work from our and other labs demonstrated that direct eye contact between two individuals can readily evoke an increased propensity to ‘mirror’ other peoples’ actions. Particularly, using transcranial magnetic stimulation (TMS), we showed that mirror-motor mapping at the level of the primary motor cortex (M1), also known as “interpersonal motor resonance” (IMR), is significantly increased upon the observation of actions accompanied by direct eye contact, compared to the observation of actions accompanied by averted eye gaze.

Objectives:  With the present study, we investigated the role of eye contact on IMR further, and in particular, explored whether administration of the ‘prosocial’ neuropeptide oxytocin (OT) can influence eye-contact induced IMR. OT is known to play an important role in promoting prosocial behavior and the perception of socially-relevant stimuli, such as eye gaze. To date however, the link between OT and IMR is less clear.

Methods: Twenty-six neurotypical adult males (18-29y) participated in a double-blind placebo-controlled cross-over design including two sessions, separated by one week. Participants were randomly assigned to receive a single dose of OT (24 IU) or placebo nasal spray at the first and second session. In each session, TMS was used to measure changes in cortico-motor excitability at the level of M1 while participants observed video stimuli of an actress performing simple hand movements combined with either direct or averted gaze. Additionally, eye tracking was performed to evaluate potential changes in spontaneous viewing behavior of the participants.

Results:  At the baseline session (after PL spray), a tentative effect of eye gaze on IMR was revealed, indicating that IMR during movement observation was higher when combined with direct eye gaze, compared to averted gaze (p=0.09). Exploration of inter-individual variance at baseline provided indications that the effect of eye gaze on IMR was related to inter-individual variance in state attachment avoidance (State Adult Attachment Measure (SAAM)), such that - at baseline - significant modulations of IMR by eye gaze were only observed in participants with low attachment avoidance (p=0.003), whereas in participants with high attachment avoidance, the facilitating effect of eye-contact on IMR was absent (p=0.50). Strikingly however, participants with high attachment avoidance that failed to display eye contact-induced IMR enhancements at baseline were shown to significantly increase eye contact-induced IMR after a single-dose of OT (p=0.043).

Conclusions:  Our results provide indications that a single-dose of OT can promote motor-mirroring of others’ movements upon direct eye contact. Particularly, in participants with high attachment avoidance, OT may increase the saliency of social cues originating from the eye regions of others, which in turn may promote the propensity of an individual to automatically ‘mirror’ the actions and behaviors of surrounding others. Overall, these findings stimulate future investigations on the potential of OT therapy for targeting eye contact avoidance in patient populations with particular implications in this domain, such as autism spectrum disorders.