Intracranial human recordings reveal association between neural activity and perceived intensity for the pain of others in the insula

  1. Efe Soyman
  2. Rune Bruls
  3. Kalliopi Ioumpa
  4. Laura Müller-Pinzler
  5. Selene Gallo
  6. Chaoyi Qin
  7. Elisabeth CW van Straaten
  8. Matthew W Self
  9. Judith C Peters
  10. Jessy K Possel
  11. Yoshiyuki Onuki
  12. Johannes C Baayen
  13. Sander Idema
  14. Christian Keysers  Is a corresponding author
  15. Valeria Gazzola  Is a corresponding author
  1. Koç University, Turkey
  2. Netherlands Institute for Neuroscience, Netherlands
  3. University of Lübeck, Germany
  4. Amsterdam University Medical Centers, Netherlands
  5. Jichi Medical University, Japan

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/

The following data sets were generated

Article and author information

Author details

  1. Efe Soyman

    Social Cognitive and Affective Neuroscience Lab, Koç University, Istanbul, Turkey
    Competing interests
    The authors declare that no competing interests exist.
  2. Rune Bruls

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Kalliopi Ioumpa

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Laura Müller-Pinzler

    Department of Psychiatry and Psychotherapy, University of Lübeck, Lübeck, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5567-5430
  5. Selene Gallo

    Department of Psychiatry, Amsterdam University Medical Centers, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Chaoyi Qin

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  7. Elisabeth CW van Straaten

    Department of Neurology and Clinical Neurophysiology, Amsterdam University Medical Centers, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  8. Matthew W Self

    Department of Vision and Cognition, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5731-579X
  9. Judith C Peters

    Department of Vision and Cognition, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  10. Jessy K Possel

    Department of Vision and Cognition, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  11. Yoshiyuki Onuki

    Department of Neurosurgery, Jichi Medical University, Tochigi, Japan
    Competing interests
    The authors declare that no competing interests exist.
  12. Johannes C Baayen

    Department of Neurosurgery, Amsterdam University Medical Centers, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  13. Sander Idema

    Department of Neurosurgery, Amsterdam University Medical Centers, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  14. Christian Keysers

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    For correspondence
    c.keysers@nin.knaw.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2845-5467
  15. Valeria Gazzola

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    For correspondence
    v.gazzola@nin.knaw.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0324-0619

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.

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.

Reviewing Editor

  1. Christian Büchel, University Medical Center Hamburg-Eppendorf, Germany

Publication history

  1. Preprint posted: June 24, 2021 (view preprint)
  2. Received: November 2, 2021
  3. Accepted: November 2, 2022
  4. Accepted Manuscript published: November 3, 2022 (version 1)
  5. 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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  1. Efe Soyman
  2. Rune Bruls
  3. Kalliopi Ioumpa
  4. Laura Müller-Pinzler
  5. Selene Gallo
  6. Chaoyi Qin
  7. Elisabeth CW van Straaten
  8. Matthew W Self
  9. Judith C Peters
  10. Jessy K Possel
  11. Yoshiyuki Onuki
  12. Johannes C Baayen
  13. Sander Idema
  14. Christian Keysers
  15. Valeria Gazzola
(2022)
Intracranial human recordings reveal association between neural activity and perceived intensity for the pain of others in the insula
eLife 11:e75197.
https://doi.org/10.7554/eLife.75197

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