Emotional content and semantic structure of dialogues are associated with Interpersonal Neural Synchrony in the Prefrontal Cortex

A fundamental characteristic of social exchanges is the synchronization of individuals' behaviors, physiological responses, and neural activity. However, the association between how individuals communicate in terms of emotional content and expressed associative knowledge and interpersonal synchrony has been scarcely investigated so far. This study addresses this research gap by bridging recent advances in cognitive neuroscience data, affective computing, and cognitive data science frameworks. Using functional near-infrared spectroscopy (fNIRS) hyperscanning, prefrontal neural data were collected during social interactions involving 84 participants (i.e., 42 dyads) aged 18-35 years. Wavelet transform coherence was used to assess interpersonal neural synchrony between participants. We used manual transcription of dialogues and automated methods to codify transcriptions as emotional levels and syntactic/semantic networks. Our quantitative findings reveal higher than random expectations levels of interpersonal neural synchrony in the superior frontal gyrus (q = .038) and the bilateral middle frontal gyri (q< .001, q< .001). Linear mixed models based on dialogues' emotional content only significantly predicted interpersonal neural synchrony across the prefrontal cortex (R<sub>marginal</sub><sup>2</sup>=3.62%). Conversely, models relying on syntactic/semantic features were more effective at the local level, for predicting brain synchrony in the right middle frontal gyrus (R<sub>marginal</sub><sup>2</sup>=9.97%). Generally, models based on the emotional content of dialogues were not effective when limited to data from one region of interest at a time, whereas models based on syntactic/semantic features show the opposite trend, losing predictive power when incorporating data from all regions of interest. Moreover, we found an interplay between emotions and associative knowledge in predicting brain synchrony, providing quantitative support to the major role played by these linguistic components in social interactions and in prefrontal processes. Our study identifies a mind-brain duality in emotions and associative knowledge reflecting neural synchrony levels, opening new ways for investigating human interactions.

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Publication Details

Journal
NeuroImage
Published
2025-02-22
DOI
https://doi.org/10.1016/j.neuroimage.2025.121087
Citations
6
Primary Topic
Action Observation and Synchronization
Type
article
Field-Weighted Citation Impact
14.63
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article

Emotional content and semantic structure of dialogues are associated with Interpersonal Neural Synchrony in the Prefrontal Cortex

Andrea Bizzego, Gianluca Esposito, Alessandro Carollo, Mengyu Lim et al.
6 citations
NeuroImage
Action Observation and Synchronization
14.63
article

Emotional content and semantic structure of dialogues are associated with Interpersonal Neural Synchrony in the Prefrontal Cortex

Andrea Bizzego, Gianluca Esposito, Alessandro Carollo, Mengyu Lim, Massimo Stella
article en
6 citations

Abstract

A fundamental characteristic of social exchanges is the synchronization of individuals' behaviors, physiological responses, and neural activity. However, the association between how individuals communicate in terms of emotional content and expressed associative knowledge and interpersonal synchrony has been scarcely investigated so far. This study addresses this research gap by bridging recent advances in cognitive neuroscience data, affective computing, and cognitive data science frameworks. Using functional near-infrared spectroscopy (fNIRS) hyperscanning, prefrontal neural data were collected during social interactions involving 84 participants (i.e., 42 dyads) aged 18-35 years. Wavelet transform coherence was used to assess interpersonal neural synchrony between participants. We used manual transcription of dialogues and automated methods to codify transcriptions as emotional levels and syntactic/semantic networks. Our quantitative findings reveal higher than random expectations levels of interpersonal neural synchrony in the superior frontal gyrus (q = .038) and the bilateral middle frontal gyri (q< .001, q< .001). Linear mixed models based on dialogues' emotional content only significantly predicted interpersonal neural synchrony across the prefrontal cortex (R<sub>marginal</sub><sup>2</sup>=3.62%). Conversely, models relying on syntactic/semantic features were more effective at the local level, for predicting brain synchrony in the right middle frontal gyrus (R<sub>marginal</sub><sup>2</sup>=9.97%). Generally, models based on the emotional content of dialogues were not effective when limited to data from one region of interest at a time, whereas models based on syntactic/semantic features show the opposite trend, losing predictive power when incorporating data from all regions of interest. Moreover, we found an interplay between emotions and associative knowledge in predicting brain synchrony, providing quantitative support to the major role played by these linguistic components in social interactions and in prefrontal processes. Our study identifies a mind-brain duality in emotions and associative knowledge reflecting neural synchrony levels, opening new ways for investigating human interactions.

NeuroImageVol. 309
Nanyang Technological University (SG), University of Trento (IT), Center for Neuroscience and Cognitive Systems (IT)
Openalex Percentile: Top 1%
Action Observation and Synchronization
14.63
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