The relationship between stability of interpersonal coordination and inter-brain EEG synchronization during anti-phase tapping

www.nature.com/scientificreports OPEN The relationship between stability of interpersonal coordination and inter‑brain EEG synchronization during anti‑phase tapping Yuto Kurihara1, Toru Takahashi2 & Rieko Osu2* Inter-brain synchronization is enhanced when individuals perform rhythmic interpersonal coordination tasks, such as playing instruments in music ensembles. Experimentally, synchronization has been shown to correlate with the performance of joint tapping tasks. However, it is unclear whether inter-brain synchronization is related to the stability of interpersonal coordination represented as the standard deviation of relative phase (SDRP). In this study, we simultaneously recorded electroencephalograms of two paired individuals during anti-phase tapping in three interactive tapping conditions: slow (reference inter-tap interval [ITI]: 0.5 s), fast (reference ITI: 0.25 s), and free (preferred ITI), and pseudo tapping where each participant tapped according to the metronome sounds without interaction. We calculated the inter-brain synchronization between pairs of six regions of interest (ROI): frontal, central, left/right temporal, parietal, and occipital regions. During the fast tapping, the inter-brain synchronization significantly increased in multiple ROI pairs including temporoparietal junction in comparison to pseudo tapping. Synchronization between the central and left-temporal regions was positively correlated with SDRP in the theta in the fast condition. These results demonstrate that inter-brain synchronization occurs when task requirements are high and increases with the instability of the coordination. People interact during group dancing and music ensembles by coordinating their actions swiftly and a ccurately1. These widespread social activities involve temporally precise interpersonal synchronization based on the information exchanged via multiple sensory modalities2. Furthermore, these social activities require that individuals coordinate stably to exhibit their p erformance3,4. Previous studies have examined the stability of interpersonal coordination using simple joint tapping tasks, such as in-phase or anti-phase tapping between two individuals4–6. Interpersonal coordination patterns can be represented by a relative phase (RP) that captures the angular differences between two o scillators7–10. The standard deviation of the relative phase (SDRP) represents the instability of the coordination patterns. Two patterns of interpersonal coordination have been examined, in-phase (RP = 0°) and anti-phase (RP = 180°) m odes11. In-phase coordination is more stable than anti-phase c oordination7,8. In particular, the anti-phase interpersonal coordination becomes increasingly unstable (increase in SDRP) as the movement frequency increases, eventually breaking down and transiting to in-phase coordination (generally called phase transition)7,12. For instance, Schmidt et al. observed that, when two participants coordinated leg movements with one another, the SDRP for the anti-phase mode was larger than that for the in-phase mode, and transition from the anti-phase to in-phase coordination was noted when the frequency of leg movement increased7. To elucidate the neural mechanisms of interpersonal coordination, hyperscanning has been used to examine the synchronization of two or more brains (inter-brain synchronization)13,14 during a variety of interaction tasks from simple joint tapping tasks15,16 to complex natural tasks, such as conversations17. Previous research demonstrates a relationship between inter-brain synchronization of electroencephalogram (EEG) signals and behavioral performance, that is, higher synchronization indicates better achievement in an interpersonal coordination 1 Graduate School of Human Sciences, Waseda University, 2‑579‑15 Mikajima, Tokorozawa, Saitama, Japan. 2Faculty of Human Sciences, Waseda University, 2‑579‑15 Mikajima, Tokorozawa, Saitama, Japan. *email: Scientific Reports | (2022) 12:6164 | https://doi.org/10.1038/s41598-022-10049-7 1 Vol.:(0123456789) www.nature.com/scientificreports/ A EEG Later Mover; participant B B First Mover; partcipant A reference ITI t1 exemplary tempo t2 t3 ITI t4 t298 t299 t300 t297 participant A participant B C anti-phase (alternative) slow condition fast condition free condition pseudo condition reference ITI=0.5 s time: 175.24±14.35 s reference ITI=0.25 s time: 116.96±10.08 s no reference ITI time: 178.94±29.44s reference ITI=0.5 s time: 178.94±29.44s Figure 1.  Experimental setting and the procedure of anti-phase tapping tasks. (A) We conducted hyperscanning using two wireless EEG systems. Each participant gazed at a fixation point in front of him/her during anti-phase tapping. (B) The anti-phase tapping tasks consisted of slow, fast, and free speed conditions. In the slow and fast conditions, the participants first listened to exemplary sounds (reference ITI) of a slow (0.5 s) and a fast (0.25 s) frequency. After the participants listened to the sound, they started to perform anti-phase tapping with the same frequency as that of the reference ITI. In the free condition, there was no reference sound. Thus, the participants performed the tapping with preferred frequency in the free condition. (C) The figure indicates the flow of the experiments. First, participants performed three interactive tapping conditions: slow, fast, and free, in that order. Then, they performed pseudo tapping conditions. task18,19. For instance, Kawasaki et al. suggested that good performance pairs of visually guided alternate tapping showed higher inter-brain EEG synchronization in the alpha frequency (12 Hz) than poor performance p airs15. These previous hyperscanning studies focused on behavioral performance representing the degree of accomplishment of the task required by the experimenter. However, none have examined the relationship between inter-brain synchronization and the stability of interpersonal coordination. If stability reflects performance and performance correlates with inter-brain EEG synchronization, inter-brain EEG synchronization would be higher when the interaction is more stable. In this study, to elucidate the relationship between the stability of interpersonal coordination and inter-brain synchronization, we examined the SDRP and inter-brain EEG synchronization during anti-phase finger tapping, which is less stable than in-phase tapping, especially when the tapping speed is i ncreased7. Nineteen pairs of participants performed anti-phase interactive finger tapping in slow (requested inter-tap interval [ITI]: 0.5 s), fast (requested ITI: 0.25 s), and free speed conditions (preferred ITI) by hearing the sounds of his and partner’s taps. The tempo was indicated by eight beeps before starting to tap (Fig. 1). Participants then performed a control condition of pseudo tapping where each participant tapped to the metronome sounds without coordinating with each other, durin (...truncated)