{"title":"Interbrain synchrony attenuation during a peer cooperative task in young children with autistic traits –an EEG hyperscanning study","authors":"I-Chun Chen , Hao-Che Hsu , Chia-Ling Chen , Meng-Han Chang , Chun-Shu Wei , Chun-Hsiang Chuang","doi":"10.1016/j.neuroimage.2025.121217","DOIUrl":null,"url":null,"abstract":"<div><div>Young children with autism spectrum disorder (ASD) traits frequently encounter difficulties in peer interaction. Assessing peer interaction performance is crucial but challenging within the clinical diagnostic paradigm of ASD. Hyperscanning, which simultaneously monitors brain activity in multiple individuals, has become a popular tool for assessing social interaction's neural features. The present study aims to investigate the brain-to-brain connectivity between child-dyads engaged in a game-like collaborative peer interaction task via the hyperscanning electroencephalogram (EEG) approach. The final sample comprised 66 young children: 18 child dyads with typical development (TD), TD-TD, and 15 with ASD traits matched to TD, TD-ASD. The study indicated a depressed level of connectivity in the dyad group with ASD as the responder, with a notable decrease observed in the beta oscillation over the right parietal to left temporal coupling between subjects. A pattern that differed from that observed in the TD-TD group was identified with regard to full-band connectivity over the right-to-right temporal region. It was observed that the TD-TD group exhibited enhanced connectivity following the completion of the task, which was not the case for the TD-ASD group. Significant correlations were observed between scores on the ASD symptom rating scale and the selected significant interbrain connectivity index. The application of a hyperscanning EEG paradigm demonstrated that the participating children with autistic traits exhibited an attenuated and apparently distinct alteration pattern of interbrain connectivity in comparison to a control group. These findings highlight the value of physiologically based measures in informing etiological and interventional studies in neuropsychiatry.</div></div>","PeriodicalId":19299,"journal":{"name":"NeuroImage","volume":"312 ","pages":"Article 121217"},"PeriodicalIF":4.7000,"publicationDate":"2025-04-15","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/S1053811925002204","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROIMAGING","Score":null,"Total":0}
引用次数: 0
Abstract
Young children with autism spectrum disorder (ASD) traits frequently encounter difficulties in peer interaction. Assessing peer interaction performance is crucial but challenging within the clinical diagnostic paradigm of ASD. Hyperscanning, which simultaneously monitors brain activity in multiple individuals, has become a popular tool for assessing social interaction's neural features. The present study aims to investigate the brain-to-brain connectivity between child-dyads engaged in a game-like collaborative peer interaction task via the hyperscanning electroencephalogram (EEG) approach. The final sample comprised 66 young children: 18 child dyads with typical development (TD), TD-TD, and 15 with ASD traits matched to TD, TD-ASD. The study indicated a depressed level of connectivity in the dyad group with ASD as the responder, with a notable decrease observed in the beta oscillation over the right parietal to left temporal coupling between subjects. A pattern that differed from that observed in the TD-TD group was identified with regard to full-band connectivity over the right-to-right temporal region. It was observed that the TD-TD group exhibited enhanced connectivity following the completion of the task, which was not the case for the TD-ASD group. Significant correlations were observed between scores on the ASD symptom rating scale and the selected significant interbrain connectivity index. The application of a hyperscanning EEG paradigm demonstrated that the participating children with autistic traits exhibited an attenuated and apparently distinct alteration pattern of interbrain connectivity in comparison to a control group. These findings highlight the value of physiologically based measures in informing etiological and interventional studies in neuropsychiatry.
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.