Oxytocin selectively modulates brain response to stimuli probing social synchrony

• Published in: NeuroImage (Orlando, Fla.) Fla.), 2016-01, Vol.124 (Pt A), p.923-930
• Main Authors: Levy, Jonathan, Goldstein, Abraham, Zagoory-Sharon, Orna, Weisman, Omri, Schneiderman, Inna, Eidelman-Rothman, Moranne, Feldman, Ruth
• Format: Article
• Language: English
• Subjects: Adult; Alpha rhythm; Alpha Rhythm - drug effects; Arousal - drug effects; Behavior; Brain - drug effects; Double-Blind Method; Humans; Magnetoencephalography; Male; Mammals; MEG; Mirror neuron network; Mirror Neurons - drug effects; Musical performances; Nerve Net - drug effects; Neural networks; Neurosciences; Oxytocin; Oxytocin - pharmacology; Parietal Lobe; Rhythm; Singers; Social Behavior; Social brain; Social synchrony; Stimulation, Chemical; Studies; Theory of Mind; Veterans; Warfare; Young Adult
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2015.09.066

The capacity to act collectively within groups has led to the survival and thriving of Homo sapiens. A central group collaboration mechanism is “social synchrony,” the coordination of behavior during joint action among affiliative members, which intensifies under threat. Here, we tested brain response to vignettes depicting social synchrony among combat veterans trained for coordinated action and following life-threatening group experience, versus controls, as modulated by oxytocin (OT), a neuropeptide supporting social synchrony. Using a randomized, double-blind, within-subject design, 40 combat-trained and control male veterans underwent magnetoencephalography (MEG) twice following OT/placebo administration while viewing two social vignettes rated as highly synchronous: pleasant male social gathering and coordinated unit during combat. Both vignettes activated a wide response across the social brain in the alpha band; the combat scene triggered stronger activations. Importantly, OT effects were modulated by prior experience. Among combat veterans, OT attenuated the increased response to combat stimuli in the posterior superior temporal sulcus (pSTS) – a hub of social perception, action observation, and mentalizing – and enhanced activation in the inferior parietal lobule (IPL) to the pleasant social scene. Among controls, OT enhanced inferior frontal gyrus (IFG) response to combat cues, demonstrating selective OT effects on mirror-neuron and mentalizing networks. OT-enhanced mirror network activity was dampened in veterans reporting higher posttraumatic symptoms. Results demonstrate that the social brain responds online, via modulation of alpha rhythms, to stimuli probing social synchrony, particularly those involving threat to survival, and OT's enhancing versus anxiolytic effects are sensitive to salient experiences within social groups. •Probing social synchrony elicits wide response across social brain in alpha band.•Response is more robust when social synchrony cues involve threat to survival.•Oxytocin selectively modulates brain response to social synchrony in mirror network.•Such selective response is shaped by prior salient experiences in social groups.