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Transient brain networks underlying interpersonal strategies during synchronized action.

ABSTRACT: Interpersonal coordination is a core part of human interaction, and its underlying mechanisms have been extensively studied using social paradigms such as joint finger-tapping. Here, individual and dyadic differences have been found to yield a range of dyadic synchronization strategies, such as mutual adaptation, leading-leading, and leading-following behaviour, but the brain mechanisms that underlie these strategies remain poorly understood. To identify individual brain mechanisms underlying emergence of these minimal social interaction strategies, we contrasted EEG-recorded brain activity in two groups of musicians exhibiting the mutual adaptation and leading-leading strategies. We found that the individuals coordinating via mutual adaptation exhibited a more frequent occurrence of phase-locked activity within a transient action-perception-related brain network in the alpha range, as compared to the leading-leading group. Furthermore, we identified parietal and temporal brain regions that changed significantly in the directionality of their within-network information flow. Our results suggest that the stronger weight on extrinsic coupling observed in computational models of mutual adaptation as compared to leading-leading might be facilitated by a higher degree of action-perception network coupling in the brain.

SUBMITTER: Heggli OA

PROVIDER: S-EPMC7812620 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Transient brain networks underlying interpersonal strategies during synchronized action.

Heggli Ole Adrian OA Konvalinka Ivana I Cabral Joana J Brattico Elvira E Kringelbach Morten L ML Vuust Peter P

Social cognitive and affective neuroscience 20210101 1-2

Interpersonal coordination is a core part of human interaction, and its underlying mechanisms have been extensively studied using social paradigms such as joint finger-tapping. Here, individual and dyadic differences have been found to yield a range of dyadic synchronization strategies, such as mutual adaptation, leading-leading, and leading-following behaviour, but the brain mechanisms that underlie these strategies remain poorly understood. To identify individual brain mechanisms underlying em ...[more]

PMID: 32337586

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Project description:Inter-brain synchronization is primarily investigated during social interactions but had not been examined during coupled muscle action between two persons until now. It was previously shown that mechanical muscle oscillations can develop coherent behavior between two isometrically interacting persons. This case study investigated if inter-brain synchronization appears thereby, and if differences of inter- and intrapersonal muscle and brain coherence exist regarding two different types of isometric muscle action. Electroencephalography (EEG) and mechanomyography/mechanotendography (MMG/MTG) of right elbow extensors were recorded during six fatiguing trials of two coupled isometrically interacting participants (70% MVIC). One partner performed holding and one pushing isometric muscle action (HIMA/PIMA; tasks changed). The wavelet coherence of all signals (EEG, MMG/MTG, force, ACC) were analyzed intra- and interpersonally. The five longest coherence patches in 8–15 Hz and their weighted frequency were compared between real vs. random pairs and between HIMA vs. PIMA. Real vs. random pairs showed significantly higher coherence for intra-muscle, intra-brain, and inter-muscle-brain activity (p < 0.001 to 0.019). Inter-brain coherence was significantly higher for real vs. random pairs for EEG of right and central areas and for sub-regions of EEG left (p = 0.002 to 0.025). Interpersonal muscle-brain synchronization was significantly higher than intrapersonal one, whereby it was significantly higher for HIMA vs. PIMA. These preliminary findings indicate that inter-brain synchronization can arise during muscular interaction. It is hypothesized both partners merge into one oscillating neuromuscular system. The results reinforce the hypothesis that HIMA is characterized by more complex control strategies than PIMA. The pilot study suggests investigating the topic further to verify these results on a larger sample size. Findings could contribute to the basic understanding of motor control and is relevant for functional diagnostics such as the manual muscle test which is applied in several disciplines, e.g., neurology, physiotherapy.

Project description:Dancing and playing music require people to coordinate actions with auditory rhythms. In laboratory perception-action coordination tasks, people are asked to synchronize taps with a metronome. When synchronizing with a metronome, people tend to anticipate stimulus onsets, tapping slightly before the stimulus. The anticipation tendency increases with longer stimulus periods of up to 3500ms, but is less pronounced in trained individuals like musicians compared to non-musicians. Furthermore, external factors influence the timing of tapping. These factors include the presence of auditory feedback from one's own taps, the presence of a partner performing coordinated joint tapping, and transmission latencies (TLs) between coordinating partners. Phenomena like the anticipation tendency can be explained by delay-coupled systems, which may be inherent to the sensorimotor system during perception-action coordination. Here we tested whether a dynamical systems model based on this hypothesis reproduces observed patterns of human synchronization. We simulated behavior with a model consisting of an oscillator receiving its own delayed activity as input. Three simulation experiments were conducted using previously-published behavioral data from 1) simple tapping, 2) two-person alternating beat-tapping, and 3) two-person alternating rhythm-clapping in the presence of a range of constant auditory TLs. In Experiment 1, our model replicated the larger anticipation observed for longer stimulus intervals and adjusting the amplitude of the delayed feedback reproduced the difference between musicians and non-musicians. In Experiment 2, by connecting two models we replicated the smaller anticipation observed in human joint tapping with bi-directional auditory feedback compared to joint tapping without feedback. In Experiment 3, we varied TLs between two models alternately receiving signals from one another. Results showed reciprocal lags at points of alternation, consistent with behavioral patterns. Overall, our model explains various anticipatory behaviors, and has potential to inform theories of adaptive human synchronization.

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Transient brain networks underlying interpersonal strategies during synchronized action.

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Transient brain networks underlying interpersonal strategies during synchronized action.

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