Perception of social synchrony induces mother-child gamma coupling in the social brain

Abstract

The recent call to move from focus on one brain's functioning to two-brain communication initiated a search for mechanisms that enable two humans to coordinate brain response during social interactions. Here, we utilized the mother-child context as a developmentally salient setting to study two-brain coupling. Mothers and their 9-year-old children were videotaped at home in positive and conflictual interactions. Positive interactions were microcoded for social synchrony and conflicts for overall dialogical style. Following, mother and child underwent magnetoencephalography while observing the positive vignettes. Episodes of behavioral synchrony, compared to non-synchrony, increased gamma-band power in the superior temporal sulcus (STS), hub of social cognition, mirroring and mentalizing. This neural pattern was coupled between mother and child. Brain-to-brain coordination was anchored in behavioral synchrony; only during episodes of behavioral synchrony, but not during non-synchronous moments, mother's and child's STS gamma power was coupled. Importantly, neural synchrony was not found during observation of unfamiliar mother-child interaction Maternal empathic/dialogical conflict style predicted mothers' STS activations whereas child withdrawal predicted attenuated STS response in both partners. Results define a novel neural marker for brain-to-brain synchrony, highlight the role of rapid bottom-up oscillatory mechanisms for neural coupling and indicate that behavior-based processes may drive synchrony between two brains during social interactions.

Keywords: MEG; gamma-band activity; magnetoencephalography; mother–child interaction; social synchrony; superior temporal sulcus.

Fig. 1.

Experimental and analytical procedures. (A) Mother–child dyads were videotaped during social interaction (left panel). Two years later mother and child were invited to participate in MEG experiment where they each observed the videotaped interaction (right panel). (B) Micro-coding in second-to-second level (left panel) to define episodes of social synchrony and non-synchrony. Global assessment of dialogical style (right panel). (C) Brain signals were extracted from the localized brain region signaling heightened activity during moments of social synchrony (compared to non-synchrony).

Fig. 2.

Brain response of mother and child to vignettes probing social synchrony. The brain response of child (left upper panel) and mother (left lower panel) to episodes of own social synchrony was expressed in the gamma-band in the right STS. The overall extent of the STS response was coupled between child and mother (middle panel). The second-by-second STS phase showed significantly greater coupling between child and mother when observing episodes of synchrony compared to episodes of non-synchrony (right panel). Color-bar illustrates masked statistical significance on the overlaid cortical surface (P_cluster-cor ≤ 0.05). *P < 0.05, **P < 0.01.

Fig. 3.

Associations between social behavior during dyadic interaction and mother’s and child’s STS activation. Behavioral empathy (left) and withdrawal (middle) correlated with mothers’ STS activation and with child’s STS activation (right). *P < 0.05.