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

Abstract 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 affectiv...

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Main Authors: J. Toppi, M. Siniatchkin, P. Vogel, C. M. Freitag, L. Astolfi, A. Ciaramidaro
Format: Article
Language:English
Published: Nature Portfolio 2022-10-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-18911-4
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author J. Toppi
M. Siniatchkin
P. Vogel
C. M. Freitag
L. Astolfi
A. Ciaramidaro
author_facet J. Toppi
M. Siniatchkin
P. Vogel
C. M. Freitag
L. Astolfi
A. Ciaramidaro
author_sort J. Toppi
collection DOAJ
description Abstract 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 doaj.art-2dd6e6bbc8774d72a2ec0d4d96971f9b2022-12-22T04:31:55ZengNature PortfolioScientific Reports2045-23222022-10-0112111210.1038/s41598-022-18911-4A novel approach to measure brain-to-brain spatial and temporal alignment during positive empathyJ. Toppi0M. Siniatchkin1P. Vogel2C. M. Freitag3L. Astolfi4A. Ciaramidaro5Department of Computer, Control and Management Engineering A. Ruberti, Sapienza University of RomeDepartment of Child and Adolescent Psychiatry and Psychotherapy, Protestant Hospital Bethel, University Clinics OWL, Campus Bethel, Bielefeld UniversityDepartment of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt, Goethe UniversityDepartment of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt, Goethe UniversityDepartment of Computer, Control and Management Engineering A. Ruberti, Sapienza University of RomeDepartment of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt, Goethe UniversityAbstract 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.https://doi.org/10.1038/s41598-022-18911-4
spellingShingle J. Toppi
M. Siniatchkin
P. Vogel
C. M. Freitag
L. Astolfi
A. Ciaramidaro
A novel approach to measure brain-to-brain spatial and temporal alignment during positive empathy
Scientific Reports
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
url https://doi.org/10.1038/s41598-022-18911-4
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