Afton M. Bierlich, Nanja T. Scheel, Leora S. Traiger, Daniel Keeser, Ralf Tepest, Alexandra L. Georgescu, Jana C. Koehler, Irene Sophia Plank, Christine M. Falter-Wagner
{"title":"社会互动感知的神经机制:观察人际同步会调节行动观察网络的激活,自闭症患者不会受到影响","authors":"Afton M. Bierlich, Nanja T. Scheel, Leora S. Traiger, Daniel Keeser, Ralf Tepest, Alexandra L. Georgescu, Jana C. Koehler, Irene Sophia Plank, Christine M. Falter-Wagner","doi":"10.1002/hbm.70052","DOIUrl":null,"url":null,"abstract":"<p>How the temporal dynamics of social interactions are perceived arguably plays an important role in how one engages in social interactions and how difficulties in establishing smooth social interactions may occur. One aspect of temporal dynamics in social interactions is the mutual coordination of individuals' behaviors during social interaction, otherwise known as behavioral interpersonal synchrony (IPS). Behavioral IPS has been studied increasingly in various contexts, such as a feature of the social interaction difficulties inherent to autism. To fully understand the temporal dynamics of social interactions, or reductions thereof in autism, the neural basis of IPS perception needs to be established. Thus, the current study's aim was twofold: to establish the basic neuro-perceptual processing of IPS in social interactions for typical observers and to test whether it might differ for autistic individuals. In a task-based fMRI paradigm, participants viewed short, silent video vignettes of humans during social interactions featuring a variation of behavioral IPS. The results show that observing behavioral IPS modulates the Action Observation Network (AON). Interestingly, autistic participants showed similar neural activation patterns as non-autistic participants which were modulated by the behavioral IPS they observed in the videos, suggesting that the perception of temporal dynamics of social interactions is spared and may not underly reduced behavioral IPS often observed in autism. Nevertheless, a general difference in processing social interactions was found in autistic observers, characterized by decreased neural activation in the right middle frontal gyrus, angular gyrus, and superior temporal areas. These findings demonstrate that although the autistic and non-autistic groups indeed differed in the neural processing of social interaction perception, the temporal dynamics of these social interactions were not the reason for these differences in social interaction perception in autism. Hence, spared recruitment of the AON for processing temporal dynamics of social interactions in autism does not account for the widely reported attenuation of IPS in autism and for the widely reported and presently observed differences in social interaction perception in autism.</p>","PeriodicalId":13019,"journal":{"name":"Human Brain Mapping","volume":"45 15","pages":""},"PeriodicalIF":3.5000,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11502411/pdf/","citationCount":"0","resultStr":"{\"title\":\"Neural Mechanisms of Social Interaction Perception: Observing Interpersonal Synchrony Modulates Action Observation Network Activation and Is Spared in Autism\",\"authors\":\"Afton M. Bierlich, Nanja T. Scheel, Leora S. Traiger, Daniel Keeser, Ralf Tepest, Alexandra L. Georgescu, Jana C. Koehler, Irene Sophia Plank, Christine M. Falter-Wagner\",\"doi\":\"10.1002/hbm.70052\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p>How the temporal dynamics of social interactions are perceived arguably plays an important role in how one engages in social interactions and how difficulties in establishing smooth social interactions may occur. One aspect of temporal dynamics in social interactions is the mutual coordination of individuals' behaviors during social interaction, otherwise known as behavioral interpersonal synchrony (IPS). Behavioral IPS has been studied increasingly in various contexts, such as a feature of the social interaction difficulties inherent to autism. To fully understand the temporal dynamics of social interactions, or reductions thereof in autism, the neural basis of IPS perception needs to be established. Thus, the current study's aim was twofold: to establish the basic neuro-perceptual processing of IPS in social interactions for typical observers and to test whether it might differ for autistic individuals. In a task-based fMRI paradigm, participants viewed short, silent video vignettes of humans during social interactions featuring a variation of behavioral IPS. The results show that observing behavioral IPS modulates the Action Observation Network (AON). Interestingly, autistic participants showed similar neural activation patterns as non-autistic participants which were modulated by the behavioral IPS they observed in the videos, suggesting that the perception of temporal dynamics of social interactions is spared and may not underly reduced behavioral IPS often observed in autism. Nevertheless, a general difference in processing social interactions was found in autistic observers, characterized by decreased neural activation in the right middle frontal gyrus, angular gyrus, and superior temporal areas. These findings demonstrate that although the autistic and non-autistic groups indeed differed in the neural processing of social interaction perception, the temporal dynamics of these social interactions were not the reason for these differences in social interaction perception in autism. Hence, spared recruitment of the AON for processing temporal dynamics of social interactions in autism does not account for the widely reported attenuation of IPS in autism and for the widely reported and presently observed differences in social interaction perception in autism.</p>\",\"PeriodicalId\":13019,\"journal\":{\"name\":\"Human Brain Mapping\",\"volume\":\"45 15\",\"pages\":\"\"},\"PeriodicalIF\":3.5000,\"publicationDate\":\"2024-10-24\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11502411/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Human Brain Mapping\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://onlinelibrary.wiley.com/doi/10.1002/hbm.70052\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"NEUROIMAGING\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Human Brain Mapping","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/hbm.70052","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROIMAGING","Score":null,"Total":0}
Neural Mechanisms of Social Interaction Perception: Observing Interpersonal Synchrony Modulates Action Observation Network Activation and Is Spared in Autism
How the temporal dynamics of social interactions are perceived arguably plays an important role in how one engages in social interactions and how difficulties in establishing smooth social interactions may occur. One aspect of temporal dynamics in social interactions is the mutual coordination of individuals' behaviors during social interaction, otherwise known as behavioral interpersonal synchrony (IPS). Behavioral IPS has been studied increasingly in various contexts, such as a feature of the social interaction difficulties inherent to autism. To fully understand the temporal dynamics of social interactions, or reductions thereof in autism, the neural basis of IPS perception needs to be established. Thus, the current study's aim was twofold: to establish the basic neuro-perceptual processing of IPS in social interactions for typical observers and to test whether it might differ for autistic individuals. In a task-based fMRI paradigm, participants viewed short, silent video vignettes of humans during social interactions featuring a variation of behavioral IPS. The results show that observing behavioral IPS modulates the Action Observation Network (AON). Interestingly, autistic participants showed similar neural activation patterns as non-autistic participants which were modulated by the behavioral IPS they observed in the videos, suggesting that the perception of temporal dynamics of social interactions is spared and may not underly reduced behavioral IPS often observed in autism. Nevertheless, a general difference in processing social interactions was found in autistic observers, characterized by decreased neural activation in the right middle frontal gyrus, angular gyrus, and superior temporal areas. These findings demonstrate that although the autistic and non-autistic groups indeed differed in the neural processing of social interaction perception, the temporal dynamics of these social interactions were not the reason for these differences in social interaction perception in autism. Hence, spared recruitment of the AON for processing temporal dynamics of social interactions in autism does not account for the widely reported attenuation of IPS in autism and for the widely reported and presently observed differences in social interaction perception in autism.
期刊介绍:
Human Brain Mapping publishes peer-reviewed basic, clinical, technical, and theoretical research in the interdisciplinary and rapidly expanding field of human brain mapping. The journal features research derived from non-invasive brain imaging modalities used to explore the spatial and temporal organization of the neural systems supporting human behavior. Imaging modalities of interest include positron emission tomography, event-related potentials, electro-and magnetoencephalography, magnetic resonance imaging, and single-photon emission tomography. Brain mapping research in both normal and clinical populations is encouraged.
Article formats include Research Articles, Review Articles, Clinical Case Studies, and Technique, as well as Technological Developments, Theoretical Articles, and Synthetic Reviews. Technical advances, such as novel brain imaging methods, analyses for detecting or localizing neural activity, synergistic uses of multiple imaging modalities, and strategies for the design of behavioral paradigms and neural-systems modeling are of particular interest. The journal endorses the propagation of methodological standards and encourages database development in the field of human brain mapping.