Oxytocin selectively modulates brain response to stimuli probing social synchrony

Jonathan Levy, Abraham Goldstein, Orna Zagoory-Sharon, Omri Weisman, Inna Schneiderman, Moranne Eidelman-Rothman, Ruth Feldman

Research output: Contribution to journalArticlepeer-review

43 Scopus citations

Abstract

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.

Original languageEnglish
Pages (from-to)923-930
Number of pages8
JournalNeuroImage
Volume124
DOIs
StatePublished - 1 Jan 2016

Bibliographical note

Publisher Copyright:
© 2015 Elsevier Inc.

Funding

Supported by grants from the Israel-German Foundation ( 1114-101.4/2010 ), the Irving B. Harris Foundation ( 2012-2014 ), the Simms–Mann Foundations ( 2014/01 ), and the I-CORE Program of the Planning and Budgeting Committee and The Israel Science Foundation (grant No. 51/11 ).

FundersFunder number
Irving B. Harris Foundation2014/01
Israel-German Foundation1114-101.4/2010
Israel Science Foundation51/11
Planning and Budgeting Committee of the Council for Higher Education of Israel

    Keywords

    • Alpha rhythm
    • MEG
    • Mirror neuron network
    • Oxytocin
    • Social brain
    • Social synchrony

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