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

IF 4.5 2区 医学 Q1 NEUROIMAGING NeuroImage Pub Date : 2025-04-01 Epub Date: 2025-02-22 DOI:10.1016/j.neuroimage.2025.121087
Alessandro Carollo , Massimo Stella , Mengyu Lim , Andrea Bizzego , Gianluca Esposito
{"title":"Emotional content and semantic structure of dialogues are associated with Interpersonal Neural Synchrony in the Prefrontal Cortex","authors":"Alessandro Carollo ,&nbsp;Massimo Stella ,&nbsp;Mengyu Lim ,&nbsp;Andrea Bizzego ,&nbsp;Gianluca Esposito","doi":"10.1016/j.neuroimage.2025.121087","DOIUrl":null,"url":null,"abstract":"<div><div>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 (<em>q</em> = .038) and the bilateral middle frontal gyri (<em>q</em> <span><math><mo>&lt;</mo></math></span> .001, <em>q</em> <span><math><mo>&lt;</mo></math></span> .001). Linear mixed models based on dialogues’ emotional content only significantly predicted interpersonal neural synchrony across the prefrontal cortex (<span><math><mrow><msubsup><mrow><mi>R</mi></mrow><mrow><mi>m</mi><mi>a</mi><mi>r</mi><mi>g</mi><mi>i</mi><mi>n</mi><mi>a</mi><mi>l</mi></mrow><mrow><mn>2</mn></mrow></msubsup><mo>=</mo><mn>3</mn><mo>.</mo><mn>62</mn><mtext>%</mtext></mrow></math></span>). Conversely, models relying on syntactic/semantic features were more effective at the local level, for predicting brain synchrony in the right middle frontal gyrus (<span><math><mrow><msubsup><mrow><mi>R</mi></mrow><mrow><mi>m</mi><mi>a</mi><mi>r</mi><mi>g</mi><mi>i</mi><mi>n</mi><mi>a</mi><mi>l</mi></mrow><mrow><mn>2</mn></mrow></msubsup><mo>=</mo><mn>9</mn><mo>.</mo><mn>97</mn><mtext>%</mtext></mrow></math></span>). 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.</div></div>","PeriodicalId":19299,"journal":{"name":"NeuroImage","volume":"309 ","pages":"Article 121087"},"PeriodicalIF":4.5000,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"NeuroImage","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1053811925000898","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/2/22 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"NEUROIMAGING","Score":null,"Total":0}
引用次数: 0

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 (Rmarginal2=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 (Rmarginal2=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.
查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
对话的情感内容和语义结构与前额叶皮层的人际神经同步有关
社会交换的一个基本特征是个体行为、生理反应和神经活动的同步性。然而,个体在情感内容和表达的联想知识方面的沟通方式与人际同步性之间的关系迄今尚未得到研究。本研究通过连接认知神经科学数据、情感计算和认知数据科学框架的最新进展来解决这一研究差距。利用功能性近红外光谱(fNIRS)超扫描技术,收集了84名年龄在18-35岁的参与者(即42对)在社交互动过程中的前额叶神经数据。用小波变换相干性评价被试之间的人际神经同步。我们使用手动转录对话和自动方法将转录编码为情感水平和句法/语义网络。我们的定量研究结果显示,在额上回(q = 0.038)和双侧额中回(q <;.001, q <;措施)。基于对话情感内容的线性混合模型仅能显著预测前额叶皮层的人际神经同步(Rmarginal2=3.62%)。相反,依赖句法/语义特征的模型在局部水平上更有效,用于预测右侧额叶中回的大脑同步(Rmarginal2=9.97%)。一般来说,基于对话情感内容的模型在一次仅限于一个感兴趣区域的数据时是无效的,而基于句法/语义特征的模型则表现出相反的趋势,在纳入所有感兴趣区域的数据时失去了预测能力。此外,我们还发现了情绪和联想知识在预测大脑同步方面的相互作用,为这些语言成分在社会互动和前额叶加工中所起的主要作用提供了定量支持。我们的研究确定了情绪和反映神经同步水平的联想知识的心脑二元性,为研究人类互动开辟了新的途径。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
NeuroImage
NeuroImage 医学-核医学
CiteScore
11.30
自引率
10.50%
发文量
809
审稿时长
63 days
期刊介绍: NeuroImage, a Journal of Brain Function provides a vehicle for communicating important advances in acquiring, analyzing, and modelling neuroimaging data and in applying these techniques to the study of structure-function and brain-behavior relationships. Though the emphasis is on the macroscopic level of human brain organization, meso-and microscopic neuroimaging across all species will be considered if informative for understanding the aforementioned relationships.
期刊最新文献
Advancing intraoperative brain mapping: First-in-human evaluation of flexible high-density electrocorticography grids for epilepsy surgery Voluntary modulation of mental effort affects the attentional shift induced by angry faces in women Comparative analysis of Heuron Brain PET and FreeSurfer software in automated amyloid quantification: Toward reproducible and clinically applicable brain PET imaging Effects of attentional instructions on neural and behavioral correlates of vocal auditory feedback control in post-stroke aphasia Multi-omics validation of myelin water fraction as a myelin-specific MRI biomarker
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1