Intranasal oxytocin enhances EEG mu rhythm desynchronization during execution and observation of social action: An exploratory study

Abstract

Intranasal administration of oxytocin (OT) has been found to facilitate prosocial behaviors, emotion recognition and cooperation between individuals. Recent electroencephalography (EEG) investigations have reported enhanced mu rhythm (alpha: 8-13 Hz; beta: 15-25 Hz) desynchronization during the observation of biological motion and stimuli probing social synchrony after the administration of intranasal OT. This hormone may therefore target a network of cortical circuits involved in higher cognitive functions, including the mirror neuron system (MNS). Here, in a double-blind, placebo-controlled, between-subjects exploratory study, we investigated whether intranasal OT modulates the cortical activity from sensorimotor areas during the observation and the execution of social and non-social grasping actions. Participants underwent EEG testing after receiving a single dose (24 IU) of either intranasal OT or placebo. Results revealed an enhancement of alpha -but not beta -desynchronization during observation and execution of social grasps, especially over central and parietal electrodes, in participants who received OT. No differences between conditions were found in the control group (CTRL). Moreover, we found a significant difference over the central-parietal region between the OT and CTRL group only within the social condition. These results suggest a possible action of intranasal OT on sensorimotor circuits involved in social perception and action understanding, which might contribute to facilitate the prosocial effects typically reported by behavioral studies.

Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development

“…Increased alpha suppression after OT administration is in keeping with adult action observation studies ( Festante et al, 2020 ; Levy et al, 2016 ; Perry et al, 2010 ) pointing to the mirror system as a neural target of OT. Classically, this system comprises premotor regions, the inferior frontal gyrus, and more posterior regions within the parietal cortex, and is involved in self-other social mapping ( Rizzolatti and Sinigaglia, 2016 ).…”

“…Significant suppression did not occur in any condition following saline administration. These results represent the first neurophysiological evidence for exogenous OT targeting cortical regions involved in social processing and socially-driven visuomotor development early in infancy, and substantiates the idea that the oxytocinergic system modulates activity in brain networks that support face perception ( Dal Monte et al, 2014 ; Liu et al, 2015 ; Taubert et al, 2019 ; Tillman et al, 2019 ) and other socio-cognitive processes ( Festante et al, 2020 ; Levy et al, 2016 ; Perry et al, 2010 ).…”

“…However, in our study, alpha suppression during the OT session was more posteriorly located, indicating that it may not, or may not exclusively, reflect sensorimotor activity, but instead could represent visual/attentional alpha modulation. In human adults, OT does increase alpha suppression over much of the scalp during action observation ( Festante et al, 2020 ; Perry et al, 2010 ), not just in central regions. An interesting possibility is that suppression in parietal locations found in our study reflects increased functional connectivity between occipital and central brain regions, and thus greater coupling of mirroring and attentional processes, which are likely to occur concurrently ( Debnath et al, 2019 ; Festante et al, 2020 ).…”

“…Adult human electroencephalography (EEG) and magnetoencephalography (MEG) studies indicate that OT also influences widespread cortical activity during social perception tasks, particularly in the alpha frequency band (8−13 Hz in adults; 5−9 Hz in infants) ( Festante et al, 2020 ; Levy et al, 2016 ; Perry et al, 2010 ). Oscillations in this frequency band are maximally expressed in amplitude (they are ‘synchronized’) during periods of rest, becoming suppressed (or desynchronized) during tasks requiring cortical engagement.…”

Correction of vasopressin deficit in the lateral septum ameliorates social deficits of mouse autism model

“…In humans, intranasal administration of AVP increased activity in the LS and reciprocated social collaboration (47). Intranasal OXT administration enhances the suppression of oscillatory activity (8-25Hz) during execution and observation of social actions (48). Altogether, OXT and AVP-dependent modulation of neural activity in response to social stimuli directly impact EEG activity, which may have a predictive value for the impact of such treatment in ASD-associated disorders.…”