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A novel approach to measure brain-to-brain spatial and temporal alignment during positive empathy

Empathy is defined as the ability to vicariously experience others’ suffering (vicarious pain) or feeling their joy (vicarious reward). While most neuroimaging studies have focused on vicarious pain and describe similar neural responses during the observed and the personal negative affective involve...

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Autores principales: Toppi, J., Siniatchkin, M., Vogel, P., Freitag, C. M., Astolfi, L., Ciaramidaro, A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9568657/
https://www.ncbi.nlm.nih.gov/pubmed/36241665
http://dx.doi.org/10.1038/s41598-022-18911-4
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author Toppi, J.
Siniatchkin, M.
Vogel, P.
Freitag, C. M.
Astolfi, L.
Ciaramidaro, A.
author_facet Toppi, J.
Siniatchkin, M.
Vogel, P.
Freitag, C. M.
Astolfi, L.
Ciaramidaro, A.
author_sort Toppi, J.
collection PubMed
description Empathy is defined as the ability to vicariously experience others’ suffering (vicarious pain) or feeling their joy (vicarious reward). While most neuroimaging studies have focused on vicarious pain and describe similar neural responses during the observed and the personal negative affective involvement, only initial evidence has been reported for the neural responses to others’ rewards and positive empathy. Here, we propose a novel approach, based on the simultaneous recording of multi-subject EEG signals and exploiting the wavelet coherence decomposition to measure the temporal alignment between ERPs in a dyad of interacting subjects. We used the Third-Party Punishment (TPP) paradigm to elicit the personal and vicarious experiences. During a positive experience, we observed the simultaneous presence in both agents of the Late Positive Potential (LPP), an ERP component related to emotion processing, as well as the existence of an inter-subject ERPs synchronization in the related time window. Moreover, the amplitude of the LPP synchronization was modulated by the presence of a human-agent. Finally, the localized brain circuits subtending the ERP-synchronization correspond to key-regions of personal and vicarious reward. Our findings suggest that the temporal and spatial ERPs alignment might be a novel and direct proxy measure of empathy.
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spelling pubmed-95686572022-10-16 A novel approach to measure brain-to-brain spatial and temporal alignment during positive empathy Toppi, J. Siniatchkin, M. Vogel, P. Freitag, C. M. Astolfi, L. Ciaramidaro, A. Sci Rep Article Empathy is defined as the ability to vicariously experience others’ suffering (vicarious pain) or feeling their joy (vicarious reward). While most neuroimaging studies have focused on vicarious pain and describe similar neural responses during the observed and the personal negative affective involvement, only initial evidence has been reported for the neural responses to others’ rewards and positive empathy. Here, we propose a novel approach, based on the simultaneous recording of multi-subject EEG signals and exploiting the wavelet coherence decomposition to measure the temporal alignment between ERPs in a dyad of interacting subjects. We used the Third-Party Punishment (TPP) paradigm to elicit the personal and vicarious experiences. During a positive experience, we observed the simultaneous presence in both agents of the Late Positive Potential (LPP), an ERP component related to emotion processing, as well as the existence of an inter-subject ERPs synchronization in the related time window. Moreover, the amplitude of the LPP synchronization was modulated by the presence of a human-agent. Finally, the localized brain circuits subtending the ERP-synchronization correspond to key-regions of personal and vicarious reward. Our findings suggest that the temporal and spatial ERPs alignment might be a novel and direct proxy measure of empathy. Nature Publishing Group UK 2022-10-14 /pmc/articles/PMC9568657/ /pubmed/36241665 http://dx.doi.org/10.1038/s41598-022-18911-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Toppi, J.
Siniatchkin, M.
Vogel, P.
Freitag, C. M.
Astolfi, L.
Ciaramidaro, A.
A novel approach to measure brain-to-brain spatial and temporal alignment during positive empathy
title A novel approach to measure brain-to-brain spatial and temporal alignment during positive empathy
title_full A novel approach to measure brain-to-brain spatial and temporal alignment during positive empathy
title_fullStr A novel approach to measure brain-to-brain spatial and temporal alignment during positive empathy
title_full_unstemmed A novel approach to measure brain-to-brain spatial and temporal alignment during positive empathy
title_short A novel approach to measure brain-to-brain spatial and temporal alignment during positive empathy
title_sort novel approach to measure brain-to-brain spatial and temporal alignment during positive empathy
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9568657/
https://www.ncbi.nlm.nih.gov/pubmed/36241665
http://dx.doi.org/10.1038/s41598-022-18911-4
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