Spontaneous dyadic behavior predicts the emergence of interpersonal neural synchrony
Synchronization of neural activity across brains – Interpersonal Neural Synchrony (INS) – is emerging as a powerful marker of social interaction that predicts success of multi-person coordination, communication, and cooperation. As the origins of INS are poorly understood, we tested whether and how...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-08-01
|
| Series: | NeuroImage |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811923003841 |
| _version_ | 1797785504272351232 |
|---|---|
| author | Atesh Koul Davide Ahmar Gian Domenico Iannetti Giacomo Novembre |
| author_facet | Atesh Koul Davide Ahmar Gian Domenico Iannetti Giacomo Novembre |
| author_sort | Atesh Koul |
| collection | DOAJ |
| description | Synchronization of neural activity across brains – Interpersonal Neural Synchrony (INS) – is emerging as a powerful marker of social interaction that predicts success of multi-person coordination, communication, and cooperation. As the origins of INS are poorly understood, we tested whether and how INS might emerge from spontaneous dyadic behavior. We recorded neural activity (EEG) and human behavior (full-body kinematics, eye movements, and facial expressions) while dyads of participants were instructed to look at each other without speaking or making co-verbal gestures. We made four fundamental observations. First, despite the absence of a structured social task, INS emerged spontaneously only when participants were able to see each other. Second, we show that such spontaneous INS, comprising specific spectral and topographic profiles, did not merely reflect intra-personal modulations of neural activity, but it rather reflected real-time and dyad-specific coupling of neural activities. Third, using state-of-art video-image processing and deep learning, we extracted the temporal unfolding of three notable social behavioral cues – body movement, eye contact, and smiling – and demonstrated that these behaviors also spontaneously synchronized within dyads. Fourth, we probed the correlates of INS in such synchronized social behaviors. Using cross-correlation and Granger causality analyses, we show that synchronized social behaviors anticipate and in fact Granger cause INS. These results provide proof-of-concept evidence for studying interpersonal neural and behavioral synchrony under natural and unconstrained conditions. Most importantly, the results suggest that INS could be conceptualized as an emergent property of two coupled neural systems: an entrainment phenomenon, promoted by real-time dyadic behavior. |
| first_indexed | 2024-03-13T00:55:00Z |
| format | Article |
| id | doaj.art-3b878a99f13c401880c7f07e01129778 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-03-13T00:55:00Z |
| publishDate | 2023-08-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-3b878a99f13c401880c7f07e011297782023-07-07T04:26:39ZengElsevierNeuroImage1095-95722023-08-01277120233Spontaneous dyadic behavior predicts the emergence of interpersonal neural synchronyAtesh Koul0Davide Ahmar1Gian Domenico Iannetti2Giacomo Novembre3Neuroscience of Perception and Action Lab, Italian Institute of Technology (IIT), Viale Regina Elena 291, Rome, Italy; Corresponding author.Neuroscience of Perception and Action Lab, Italian Institute of Technology (IIT), Viale Regina Elena 291, Rome, ItalyNeuroscience and Behavior Lab, Italian Institute of Technology (IIT), Viale Regina Elena 291, Rome, Italy; Department of Neuroscience, Physiology and Pharmacology, University College London (UCL), WC1E 6BT London, UKNeuroscience of Perception and Action Lab, Italian Institute of Technology (IIT), Viale Regina Elena 291, Rome, ItalySynchronization of neural activity across brains – Interpersonal Neural Synchrony (INS) – is emerging as a powerful marker of social interaction that predicts success of multi-person coordination, communication, and cooperation. As the origins of INS are poorly understood, we tested whether and how INS might emerge from spontaneous dyadic behavior. We recorded neural activity (EEG) and human behavior (full-body kinematics, eye movements, and facial expressions) while dyads of participants were instructed to look at each other without speaking or making co-verbal gestures. We made four fundamental observations. First, despite the absence of a structured social task, INS emerged spontaneously only when participants were able to see each other. Second, we show that such spontaneous INS, comprising specific spectral and topographic profiles, did not merely reflect intra-personal modulations of neural activity, but it rather reflected real-time and dyad-specific coupling of neural activities. Third, using state-of-art video-image processing and deep learning, we extracted the temporal unfolding of three notable social behavioral cues – body movement, eye contact, and smiling – and demonstrated that these behaviors also spontaneously synchronized within dyads. Fourth, we probed the correlates of INS in such synchronized social behaviors. Using cross-correlation and Granger causality analyses, we show that synchronized social behaviors anticipate and in fact Granger cause INS. These results provide proof-of-concept evidence for studying interpersonal neural and behavioral synchrony under natural and unconstrained conditions. Most importantly, the results suggest that INS could be conceptualized as an emergent property of two coupled neural systems: an entrainment phenomenon, promoted by real-time dyadic behavior.http://www.sciencedirect.com/science/article/pii/S1053811923003841Behavioral synchronySpontaneous behaviorVideo-based analysisEEGHyperscanningSocial interaction |
| spellingShingle | Atesh Koul Davide Ahmar Gian Domenico Iannetti Giacomo Novembre Spontaneous dyadic behavior predicts the emergence of interpersonal neural synchrony NeuroImage Behavioral synchrony Spontaneous behavior Video-based analysis EEG Hyperscanning Social interaction |
| title | Spontaneous dyadic behavior predicts the emergence of interpersonal neural synchrony |
| title_full | Spontaneous dyadic behavior predicts the emergence of interpersonal neural synchrony |
| title_fullStr | Spontaneous dyadic behavior predicts the emergence of interpersonal neural synchrony |
| title_full_unstemmed | Spontaneous dyadic behavior predicts the emergence of interpersonal neural synchrony |
| title_short | Spontaneous dyadic behavior predicts the emergence of interpersonal neural synchrony |
| title_sort | spontaneous dyadic behavior predicts the emergence of interpersonal neural synchrony |
| topic | Behavioral synchrony Spontaneous behavior Video-based analysis EEG Hyperscanning Social interaction |
| url | http://www.sciencedirect.com/science/article/pii/S1053811923003841 |
| work_keys_str_mv | AT ateshkoul spontaneousdyadicbehaviorpredictstheemergenceofinterpersonalneuralsynchrony AT davideahmar spontaneousdyadicbehaviorpredictstheemergenceofinterpersonalneuralsynchrony AT giandomenicoiannetti spontaneousdyadicbehaviorpredictstheemergenceofinterpersonalneuralsynchrony AT giacomonovembre spontaneousdyadicbehaviorpredictstheemergenceofinterpersonalneuralsynchrony |