Inter-brain synchronization during social interaction

Abstract

During social interaction, both participants are continuously active, each modifying their own actions in response to the continuously changing actions of the partner. This continuous mutual adaptation results in interactional synchrony to which both members contribute. Freely exchanging the role of imitator and model is a well-framed example of interactional synchrony resulting from a mutual behavioral negotiation. How the participants' brain activity underlies this process is currently a question that hyperscanning recordings allow us to explore. In particular, it remains largely unknown to what extent oscillatory synchronization could emerge between two brains during social interaction. To explore this issue, 18 participants paired as 9 dyads were recorded with dual-video and dual-EEG setups while they were engaged in spontaneous imitation of hand movements. We measured interactional synchrony and the turn-taking between model and imitator. We discovered by the use of nonlinear techniques that states of interactional synchrony correlate with the emergence of an interbrain synchronizing network in the alpha-mu band between the right centroparietal regions. These regions have been suggested to play a pivotal role in social interaction. Here, they acted symmetrically as key functional hubs in the interindividual brainweb. Additionally, neural synchronization became asymmetrical in the higher frequency bands possibly reflecting a top-down modulation of the roles of model and imitator in the ongoing interaction.

Figure 1. Experimental design and coding software.

A. Apparatus and experimental setting of the double video system and dual-EEG recording. B. ELAN software window during an indexing session.

Figure 2. Intersubject neural synchronizations during interactional synchrony.

Representation of statistically significant (P<0.05, nonparametric permutation test, corrected for multiple comparisons) coupling (PLV) for all subjects between electrodes of the model and the imitator: comparison for spontaneous imitation trials between behavioral synchrony episodes and those with no behavioral synchrony (Sync vs. NSync). On the left of the figures the participants are models, on the right the participants are imitators. A. Alpha-Mu band cluster between right centro-parietal regions. B. Beta band cluster between central and right parieto-occipital regions. C. Gamma band cluster between centroparietal and parieto-occipital regions.

Figure 3. Brain synchronization: online example.

Samples of spontaneous imitation episodes in the dyad n°3 showing the correspondence between interactional synchrony and brain activities. The green areas indicate periods where subjects were behaviorally synchronized and the red ones periods without behavioral synchrony. A. Time course of normalized EEG signal filtered in the alpha-mu frequency band for the channels P8 of both subjects. These channels are members of the cluster shown in figure 2A. B. Phase extracted from the signals. C. PLV calculated with sliding centred time windows of 800ms length in the alpha-mu band (related to A and B) quantifying the neural synchronization between the two subjects. Beta band PLV for the same electrodes is also shown in dashed line. D. Time course of normalized EEG signal filtered in alpha-mu frequency band for the channels PO2 in Subject 1 and Cz in Subject 2. Those channels are not members of any clusters. E. Phase extracted from the signals. F. PLV calculated with sliding centred time windows of 800ms length in the alpha-mu band (related to D and E) quantifying the neural synchronization between the two subjects. Beta band PLV for the same electrodes is also shown in dashed line. G Representation of the pairs of electrodes P8-P8 (A,B,C) and PO2-Cz (D,E,F).

Figure 4. Summary of relevant intersubject synchronizations for all dyads according to interactional synchrony.

cPLV values indicate the averaged PLVs on all pairs of electrodes members of clusters shown in Figure 2. Averages cPLV across dyads are shown in black dashed lines.

Figure 5. Averaged intersubject clustered PLV (cPLV) difference between synchronous and non-synchronous interactions (Sync - NSync) compared for experimental and surrogate behavioral analysis.

Bars represent standard errors.