Intracranial human recordings reveal association between neural activity and perceived intensity for the pain of others in the insula
Abstract
Based on neuroimaging data, the insula is considered important for people to empathize with the pain of others. Here we present intracranial electroencephalographic (iEEG) recordings and single-cell recordings from the human insulae while 7 epilepsy patients rated the intensity of a woman's painful experiences seen in short movie clips. Pain had to be deduced from seeing facial expressions or a hand being slapped by a belt. We found activity in the broadband 20-190 Hz range correlated with the trial-by-trial perceived intensity in the insula for both types of stimuli. Within the insula, some locations had activity correlating with perceived intensity for our facial expressions but not for our hand stimuli, others only for our hand but not our face stimuli, and others for both. The timing of responses to the sight of the hand being hit is best explained by kinematic information; that for our facial expressions, by shape information. Comparing the broadband activity in the iEEG signal with spiking activity from a small number of neurons and an fMRI experiment with similar stimuli, revealed a consistent spatial organization, with stronger associations with intensity more anteriorly, while viewing the hand being slapped.
Data availability
The data presented in this work is publicly available at the Open Science Framework: https://osf.io/mcahz/
Article and author information
Author details
Funding
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (452-14-015)
- Valeria Gazzola
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (453-15-009)
- Christian Keysers
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Christian Büchel, University Medical Center Hamburg-Eppendorf, Germany
Ethics
Human subjects: Written informed consent was obtained from each participant before participating in the study. All procedures on patients were approved by the medical ethical committee of the Vrije University Medical Center (protocol 2016/037). All procedures on healthy participants were approved by the local ethics committee of the University of Amsterdam (protocols 2017-EXT-8542 and 2021-EXT-13608). In addition, written informed consent to publish was obtained from the individual whose photographs are shown in Figures 1 and 3 of the article.
Version history
- Preprint posted: June 24, 2021 (view preprint)
- Received: November 2, 2021
- Accepted: November 2, 2022
- Accepted Manuscript published: November 3, 2022 (version 1)
- Version of Record published: November 21, 2022 (version 2)
Copyright
© 2022, Soyman et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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