Edited by:
Reviewed by:
*Correspondence:
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
We walk together, we watch together, we win together: Interpersonally coordinated actions are omnipresent in everyday life, yet the associated neural mechanisms are not well understood. Available evidence suggests that the synchronization of oscillatory activity across brains may provide a mechanism for the temporal alignment of actions between two or more individuals. In an attempt to provide a direct test of this hypothesis, we applied transcranial alternating current stimulation simultaneously to two individuals (hyper-tACS) who were asked to drum in synchrony at a set pace. Thirty-eight female-female dyads performed the dyadic drumming in the course of 3 weeks under three different hyper-tACS stimulation conditions: same-phase-same-frequency; different-phase-different-frequency; sham. Based on available evidence and theoretical considerations, stimulation was applied over right frontal and parietal sites in the theta frequency range. We predicted that same-phase-same-frequency stimulation would improve interpersonal action coordination, expressed as the degree of synchrony in dyadic drumming, relative to the other two conditions. Contrary to expectations, both the same-phase-same-frequency and the different-phase-different-frequency conditions were associated with greater dyadic drumming asynchrony relative to the sham condition. No influence of hyper-tACS on behavioral performance was seen when participants were asked to drum separately in synchrony to a metronome. Individual and dyad preferred drumming tempo was also unaffected by hyper-tACS. We discuss limitations of the present version of the hyper-tACS paradigm, and suggest avenues for future research.
Joint actions abound in everyday life. When passing plates at the dinner table, when enjoying card games or when playing music together (
Recent interaction experiments using EEG-hyperscanning, the simultaneous recording of multiple persons’ EEG signals (
Transcranial alternating current stimulation (tACS) seems well suited for this purpose. A growing body of studies has shown that tACS is able to modify cortical excitability and activity as well as behavioral performance in various domains, such as memory, learning, or motor function (
Overall, there is consensus in the literature that tACS affects local and possibly remote oscillatory activity. Applying tACS at frequencies in the EEG range entrains neuronal networks at the applied frequency (
In the present study, we adapted the logic of the
In order to exert a high degree of experimental control while maintaining the ecological validity and continuous interaction of musical performance paradigms (
Very recently,
However, inter-brain coupling at
In this study we applied hyper-tACS during dyadic drumming to manipulate ongoing inter-brain synchronization to study the effect of this manipulation on interpersonal action synchronization. We hypothesized that if inter-brain oscillatory couplings are indeed constitutive for joint action, experimental modulation of inter-brain oscillatory synchronization would affect the degree of interpersonal action coordination.
In particular, we hypothesized that same-phase-same-frequency hyper-tACS would improve dyadic drumming synchronization, while different-phase-different-frequency hyper-tACS would harm dyadic drumming synchronization. Moreover, we also expected that hyper-tACS would not affect behavioral performance when synchronizing to a metronome, as our stimulation did not target motor processes in the left hemisphere, but coordination processes assumed to reside in the right hemisphere. We furthermore included metronome frequencies harmonic to the stimulation frequencies to control for any potential purely motor impact of the tACS on drumming performance at corresponding harmonic frequencies.
Initially, 44 female–female dyads participated in the study. Six of the 44 dyads discontinued the experiment, for reasons unrelated to drumming or synchronization performance. Thus, the effective sample consisted of 38 female–female dyads (age range: 20–30 years, mean = 24 years, standard deviation = 2.8 years). Participants did not know each other prior to the study. We decided to include only female participants to prevent effects due to differences in the sex composition of the dyads (
All participants volunteered for the experiment and gave written informed consent prior to their inclusion in the study. The Ethics Committee of the German Psychology Society approved the study. The study was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.
Participant pairs were seated back-to-back in an electromagnetically shielded cabin with a portable wall separating both participants. This setup was used to exclude non-verbal communication cues and to allow a relatively tight control of interaction parameters, as the entire flow of information within the dyad was contained in the temporal distribution of the drum beats. Both participants drummed with the drumsticks in their right hands. Drum beats were digitized (Roland drum computer, Germany), and along with auditory instructions and metronome beats (both sent from Intel Xeon, 3.7 GHz PC running Windows 7) played to participants through in-ear headphones, covered by additional soundproof headphones. Drum beat data was recorded from two redundant sources. First, sensors (BIOVISION; single axis, sensitivity: 50 g) attached to the top end of the drumsticks recorded drumstick acceleration, and a peak detection algorithm was used to determine at which exact time points (in milliseconds) drum beats occurred. Second, the digitized drum beat signals were recorded directly via an ExG bipolar amplifier (Brain Products, Munich, Germany) on a second PC (Intel Core i5, 3.2 GHz running Windows XP). Due to technical problems with the acceleration sensors and the higher accuracy of the auditory signal, only the drum beat time series derived from the digitized drum beats were used for further analyses. TACS electrodes were placed first and EEG-electrodes were placed on all sites of a 32-electrodes setup according to the international 10–20 system that were not covered by the tACS electrodes. EEG was thus recorded from both participants with active 21 Ag/AgCl electrodes per person, with the reference electrode at the right mastoid (actiCAP, Brain Products, Munich, Germany). EEG data were collected for a different study, for the present report no EEG data have been analyzed as removal of the tACS-induced EEG-artifact is non-trival.
The dyadic drumming paradigm used in this study (see
Experimental set-up of the dyadic drumming paradigm. Participants sat back-to-back, were separated by a portable wall and drummed in symmetrical synchrony with each other or with a metronome while receiving hyper-tACS. Drum beats were digitized via the drum computer and along with auditory instructions and metronome beats sent from the PC to the participants’ headphones. Acceleration sensors were placed on the drum sticks. Cable connections depicted in gray.
All instructions and drum/metronome beats were delivered through headphones. Each trial was prefaced with a word that indicated the condition of the following trial (‘joint’/‘metronome’/‘individual’), followed by a beep that signaled the trial start. After 16 s trial duration, the trial end was signaled by another beep. Subsequently, participants replied to the post-trial questions by button presses. There was one post-trial question for both non-dyadic conditions ‘How stable was the frequency of drumming?’ for individual trials (1 = bad, 2 = ok, 3 = good) and ‘How well did the synchronization go?’ for metronome trials (1 = bad, 2 = ok, 3 = good). After dyadic trials, participants answered two questions: ‘How well did the synchronization go?’ (1 = bad, 2 = ok, 3 = good) and ‘Who determined the frequency of drumming?’ (1 = me, 2 = both 3 = other).
To assess the influence of hyper-tACS on dyadic, metronome and individual drumming we conducted a multiple-session study. Each dyad visited the lab for three experimental sessions, separated by 1 week each. Experimental sessions differed only in hyper-tACS parameter and each session consisted of three segments: pre-stimulation (pre), hyper-tACS stimulation (stimulation), and post-stimulation (post). The pre and post segments were identical and consisted of 21 trials each (five individual, eight dyadic, eight metronome; dyadic and metronome trials alternated in blocks of four trials). To maximize dyadic drumming trials during the stimulation segment, this segment consisted of 45 trials (seven individual, thirty dyadic, and eight metronome; blocks of three dyadic trials were separated by one individual/metronome trial in a pseudorandomized order). Session length varied slightly depending on each dyad’s speed of answering the post-trial questions. Pre and post lasted 10–12 min each and stimulation lasted 21–25 min (variance is due to dyad’s differential response speed to post-trial questions). Participants took a short break between pre and stimulation and between stimulation and post.
We used a measure of dyadic drumming asynchrony previously established in our lab, referred to as ‘asynchrony score’ (for details, see
Electrical stimulation was delivered through a four-channel direct current stimulator (DC-Stimulator MC; NeuroConn GmbH, Ilmenau, Germany). The tACS stimulator was connected to three conductive rubber electrodes (each 5 cm × 5 cm). Similar to the setup used by
Organization of different stimulation types across sessions.
Group | Session 1 | Session 2 | Session 3 |
---|---|---|---|
A (13 dyads) | Different | Sham | Same |
B (13 dyads) | Same | Different | Sham |
C (12 dyads) | Sham | Same | Different |
We used (
Visual inspection of residual plots did not reveal any obvious deviations from homoscedasticity or normality.
Linear mixed model analysis showed differential effects for conditions (combination of stimulation type and experimental segment) on dyadic asynchrony [χ2(6) = 60.21,
Results of the fixed effect of the linear mixed model analysis for the effect of condition on dyadic and metronome asynchrony scores. Displayed are mean asynchrony scores as estimated by the model. Stimulation conditions: Pre, pre; S Stim, sham stimulation; S-F Stim, same-phase-same-frequency stimulation; D-F Stim, different-phase-different-frequency stimulation; S Post, sham post; S-F Post, same-phase-same-frequency post; D-F Post, different-phase-different-frequency post. Standard errors are indicated by horizontal lines.
Results of the fixed effect of the linear mixed model analysis for the effect of condition on asynchrony scores.
Linear mixed model analysis showed differential effects for conditions (combination of stimulation type and experimental segment) on metronome asynchrony [χ2(6) = 146.65,
Results of the fixed effect of the linear mixed model analysis for the effect of condition on asynchrony scores.
Mean individual preferred inter-tap interval across all experimental segments and sessions was 593.21 ms (
Comparison of the fixed effect results of the linear mixed model analysis for the effect of condition on individual preferred and dyadic preferred drumming tempo for all experimental conditions. Displayed are mean inter-drum intervals as estimated by the model. Stimulation conditions: Pre, pre; S Stim, sham stimulation; S-F Stim, same-phase-same-frequency stimulation; D-F Stim, different-phase-different-frequency stimulation; S Post, sham post; S-F Post, same-phase-same-frequency post; D-F Post, different-phase-different-frequency post. Standard errors are indicated by horizontal lines.
Results of the fixed effect of the linear mixed model analysis for the effect of condition on individual and dyadic preferred drumming tempo.
Preferred tempo also did not differ between same-phase-same-frequency and different-phase-different-frequency post-stimulation [
Mean dyad preferred inter-tap interval across all experimental segments and sessions was 515.06 ms (
The aim of the present study was to investigate how manipulation of ongoing inter-brain phase synchronization by hyper-tACS would affect the synchrony of dyadic drumming performance. Previous research showed that the real-time neural dynamics of various forms of interpersonally coordinated behavior are characterized by inter-brain phase synchronization (
The main result of the present study is that, compared to sham stimulation, only dyadic asynchrony was modulated by same-phase-same-frequency and different-phase-different-frequency hyper-tACS. Metronome asynchrony, individual preferred tempo and dyad preferred tempo were not modulated. Performance on all four behavioral measures changed between pre-stimulation and stimulation, and between stimulation and post-stimulation conditions under sham hyper-tACS: Dyadic asynchrony decreased while metronome asynchrony increased, and both individuals and dyads preferred faster tempi (see
Inter-brain synchronization appears to play a functional role in establishing interpersonally coordinated actions.
Contrary to our guiding hypothesis, we did not observe a differential effect of same-phase-same-frequency and different-phase-different-frequency hyper-tACS on dyadic drumming performance. It is possible that this results from person-to-person variation in the actual frequency of neural entrainment caused by tACS stimulation. It is known that tACS stimulation of a single location may produce a range of different effects at the neural level. For example, 10 Hz tACS applied over the motor cortex inhibits motor evoked potential but improves visuo-motor implicit learning (
We did not observe any performance increases when participants drummed in synchrony with a metronome whose frequency was harmonic to the tACS frequency. This null result might either be taken to support our operationalization to target coordination rather than pure motor processes, or to support the interpretation that hyper-tACS was not successful in boosting the same frequencies in both brains. While “there is need of online tACS/EEG evidence to open a new frontier in oscillatory brain rhythms investigations” (
Further, correlations between behavioral performance and synchrony in inter-brain dynamics have only been reported in a few studies and often did not follow a linear ‘more is better’ principle. In a study using a turn-based card game paradigm,
The range of individual preferred tempo found in the present study is comparable to the range reported in the literature (
To our knowledge, dyad preferred tempo, its relation to the tempi preferred by the two individuals within the dyad and its stability over time has not been systematically studied in a tapping or drumming paradigm yet. Interestingly, dyad preferred tempo was generally faster than preferred tempo in individual drumming. Like individual-preferred tempo, it increased after the pre-stimulation, potentially as a function of time (compare 9). Though faster, dyad-preferred tempi were characterized by lower inter-trial variance than individual-preferred tempi. The fact that preferred tempo increased when drumming dyadically may relate to the suggestion that interacting individuals decrease their temporal variability in an effort to make themselves more predictable and thus facilitate joint action (
Due to methodological challenges in controlling current flow and precise neural entrainment with tACS, this present pioneering study lacks a validation to what degree the neural frequencies of the interacting participants become more synchronized or desynchronized upon hyper-tACS. Thanks to recent advances in the field of non-invasive brain stimulation stimulation protocols that circumvent stimulation artifacts have been introduced, such as amplitude-modulated tACS (
The stimulation protocol chosen further limits this study in that stimulation was delivered only to frontocentral and centroparietal areas in the right hemisphere at specific frequencies in the theta range. Future research is needed to verify if similar results could be obtained with different stimulation frequencies within the theta range. This setup might have prevented us from detecting effects of hyper-tACS on synchronization phenomena closer to the motor level. In a recent study
The present study is an attempt to experimentally manipulate inter-brain dynamics and observe the effects of this manipulation on joint action performance. We operationalized this goal by applying same-phase-same-frequency and different-phase-different-frequency hyper-tACS during a dyadic drumming paradigm, where dyads were instructed to drum in synchrony with another participant. Contrary to expectations, we found a reduction in dyadic synchrony during active hyper-tACS when compared to sham tACS. This reduction was not evident when individuals were asked to synchronize to a metronome, nor paralleled by corresponding changes in dyadic drumming frequency or individual preferred tempo.
We suspect that the observed impairment in dyadic drumming synchrony in the same-phase-same-frequency tACS condition may reflect individual differences in the frequency entrainment induced by tACS. Further hyper-tACS studies with more precise stimulation protocols are needed that ensure oscillations in the same frequencies are entrained in the brains of two individuals engaging in joint action.
As a byproduct of the paradigm used, we observed specific relationships between individual and dyad preferred drumming tempi. The tempi preferred by the two individuals in a dyad predicted the dyad’s preferred tempo. However, the dyad’s preferred tempo was generally characterized by lower variance and higher frequencies than the tempi preferred by the individuals alone. The interplay between individual- and dyad-preferred drumming or tapping tempo might present a useful clues for a more mechanistic understanding of interpersonal action coordination.
This study was carried out in accordance with the recommendations of Deutsche Gesellschaft für Psychologie with written informed consent from all subjects. All subjects gave written informed consent in accordance with the Declaration of Helsinki. The protocol was approved by the Deutsche Gesellschaft für Psychologie.
CS, TB, VM, and UL designed the experiment. CS acquired the data. CS and TvO analyzed the data. CS, TB, VM, and UL interpreted the data. CS, TB, VM, and UL wrote the manuscript. CS, TB, VM, TvO, and UL approved the final version of the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors are grateful to Douglas Garrett for conceptual considerations, to Anna Würtz, Melinda Mende, and Shiva Motlagh for their help with data acquisition and to Berndt Wischnewski for his technical support.
The Supplementary Material for this article can be found online at:
The setup by