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Rapid Processing of Observed Touch through Social Perceptual Brain Regions: An EEG-fMRI Fusion Study

Seeing social touch triggers a strong social-affective response that involves multiple brain networks, including visual, social perceptual, and somatosensory systems. Previous studies have identified the specific functional role of each system, but little is known about the speed and directionality...

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Autores principales: Lee Masson, Haemy, Isik, Leyla
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10634570/
https://www.ncbi.nlm.nih.gov/pubmed/37871963
http://dx.doi.org/10.1523/JNEUROSCI.0995-23.2023
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author Lee Masson, Haemy
Isik, Leyla
author_facet Lee Masson, Haemy
Isik, Leyla
author_sort Lee Masson, Haemy
collection PubMed
description Seeing social touch triggers a strong social-affective response that involves multiple brain networks, including visual, social perceptual, and somatosensory systems. Previous studies have identified the specific functional role of each system, but little is known about the speed and directionality of the information flow. Is this information extracted via the social perceptual system or from simulation from somatosensory cortex? To address this, we examined the spatiotemporal neural processing of observed touch. Twenty-one human participants (seven males) watched 500-ms video clips showing social and nonsocial touch during electroencephalogram (EEG) recording. Visual and social-affective features were rapidly extracted in the brain, beginning at 90 and 150 ms after video onset, respectively. Combining the EEG data with functional magnetic resonance imaging (fMRI) data from our prior study with the same stimuli reveals that neural information first arises in early visual cortex (EVC), then in the temporoparietal junction and posterior superior temporal sulcus (TPJ/pSTS), and finally in the somatosensory cortex. EVC and TPJ/pSTS uniquely explain EEG neural patterns, while somatosensory cortex does not contribute to EEG patterns alone, suggesting that social-affective information may flow from TPJ/pSTS to somatosensory cortex. Together, these findings show that social touch is processed quickly, within the timeframe of feedforward visual processes, and that the social-affective meaning of touch is first extracted by a social perceptual pathway. Such rapid processing of social touch may be vital to its effective use during social interaction. SIGNIFICANCE STATEMENT Seeing physical contact between people evokes a strong social-emotional response. Previous research has identified the brain systems responsible for this response, but little is known about how quickly and in what direction the information flows. We demonstrated that the brain processes the social-emotional meaning of observed touch quickly, starting as early as 150 ms after the stimulus onset. By combining electroencephalogram (EEG) data with functional magnetic resonance imaging (fMRI) data, we show for the first time that the social-affective meaning of touch is first extracted by a social perceptual pathway and followed by the later involvement of somatosensory simulation. This rapid processing of touch through the social perceptual route may play a pivotal role in effective usage of touch in social communication and interaction.
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spelling pubmed-106345702023-11-15 Rapid Processing of Observed Touch through Social Perceptual Brain Regions: An EEG-fMRI Fusion Study Lee Masson, Haemy Isik, Leyla J Neurosci Research Articles Seeing social touch triggers a strong social-affective response that involves multiple brain networks, including visual, social perceptual, and somatosensory systems. Previous studies have identified the specific functional role of each system, but little is known about the speed and directionality of the information flow. Is this information extracted via the social perceptual system or from simulation from somatosensory cortex? To address this, we examined the spatiotemporal neural processing of observed touch. Twenty-one human participants (seven males) watched 500-ms video clips showing social and nonsocial touch during electroencephalogram (EEG) recording. Visual and social-affective features were rapidly extracted in the brain, beginning at 90 and 150 ms after video onset, respectively. Combining the EEG data with functional magnetic resonance imaging (fMRI) data from our prior study with the same stimuli reveals that neural information first arises in early visual cortex (EVC), then in the temporoparietal junction and posterior superior temporal sulcus (TPJ/pSTS), and finally in the somatosensory cortex. EVC and TPJ/pSTS uniquely explain EEG neural patterns, while somatosensory cortex does not contribute to EEG patterns alone, suggesting that social-affective information may flow from TPJ/pSTS to somatosensory cortex. Together, these findings show that social touch is processed quickly, within the timeframe of feedforward visual processes, and that the social-affective meaning of touch is first extracted by a social perceptual pathway. Such rapid processing of social touch may be vital to its effective use during social interaction. SIGNIFICANCE STATEMENT Seeing physical contact between people evokes a strong social-emotional response. Previous research has identified the brain systems responsible for this response, but little is known about how quickly and in what direction the information flows. We demonstrated that the brain processes the social-emotional meaning of observed touch quickly, starting as early as 150 ms after the stimulus onset. By combining electroencephalogram (EEG) data with functional magnetic resonance imaging (fMRI) data, we show for the first time that the social-affective meaning of touch is first extracted by a social perceptual pathway and followed by the later involvement of somatosensory simulation. This rapid processing of touch through the social perceptual route may play a pivotal role in effective usage of touch in social communication and interaction. Society for Neuroscience 2023-11-08 /pmc/articles/PMC10634570/ /pubmed/37871963 http://dx.doi.org/10.1523/JNEUROSCI.0995-23.2023 Text en Copyright © 2023 Lee Masson and Isik https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Lee Masson, Haemy
Isik, Leyla
Rapid Processing of Observed Touch through Social Perceptual Brain Regions: An EEG-fMRI Fusion Study
title Rapid Processing of Observed Touch through Social Perceptual Brain Regions: An EEG-fMRI Fusion Study
title_full Rapid Processing of Observed Touch through Social Perceptual Brain Regions: An EEG-fMRI Fusion Study
title_fullStr Rapid Processing of Observed Touch through Social Perceptual Brain Regions: An EEG-fMRI Fusion Study
title_full_unstemmed Rapid Processing of Observed Touch through Social Perceptual Brain Regions: An EEG-fMRI Fusion Study
title_short Rapid Processing of Observed Touch through Social Perceptual Brain Regions: An EEG-fMRI Fusion Study
title_sort rapid processing of observed touch through social perceptual brain regions: an eeg-fmri fusion study
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10634570/
https://www.ncbi.nlm.nih.gov/pubmed/37871963
http://dx.doi.org/10.1523/JNEUROSCI.0995-23.2023
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