Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain

Abstract

Empathy for pain engages both shared affective responses and self-other distinction. In this study, we addressed the highly debated question of whether neural responses previously linked to affect sharing could result from the perception of salient affective displays. Moreover, we investigated how the brain network involved in affect sharing and self-other distinction underpinned our response to a pain that is either perceived as genuine or pretended (while in fact both were acted for reasons of experimental control). We found stronger activations in regions associated with affect sharing (anterior insula, aIns, and anterior mid-cingulate cortex, aMCC) as well as with affective self-other distinction (right supramarginal gyrus, rSMG), in participants watching video clips of genuine vs. pretended facial expressions of pain. Using dynamic causal modeling (DCM), we then assessed the neural dynamics between the right aIns and rSMG in these two conditions. This revealed a reduced inhibitory effect on the aIns to rSMG connection for genuine compared to pretended pain. For genuine pain only, brain-to-behavior regression analyses highlighted a linkage between this inhibitory effect on the one hand, and pain ratings as well as empathic traits on the other. These findings imply that if the pain of others is genuine and thus calls for an appropriate empathic response, neural responses in the aIns indeed seem related to affect sharing and self-other distinction is engaged to avoid empathic over-arousal. In contrast, if others merely pretend to be in pain, the perceptual salience of their painful expression results in neural responses that are down-regulated to avoid inappropriate affect sharing and social support.

Data availability

All data needed to evaluate the conclusions in the paper are present in the paper. Raw functional imaging and behavioral data are deposited at https://doi.org/10.5281/zenodo.4783235. Processed behavioral data and individual DCM parameters are accessible at https://github.com/Yili-Zhao/Genuine_pretended-pain-task.git. Unthresholded statistical maps are available at https://identifiers.org/neurovault.collection:9949.

Article and author information

Author details

  1. Yili Zhao

    Department of Cognition, Emotion, and Methods in Psychology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4535-6636
  2. Lei Zhang

    Faculty of Psychology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9586-595X
  3. Markus Rütgen

    Faculty of Psychology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4947-7734
  4. Ronald Sladky

    Faculty of Psychology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5986-1572
  5. Claus Lamm

    Department of Cognition, Emotion, and Methods in Psychology, University of Vienna, Vienna, Austria
    For correspondence
    claus.lamm@univie.ac.at
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5422-0653

Funding

Chinese Scholarship Council (Graduate Student Fellowship,201604910515)

  • Yili Zhao

Vienna Doctoral School in Cognition, Behavior and Neuroscience (Dissertation Completion Fellowship)

  • Yili Zhao

Vienna Science and Technology Fund (WWTF VRG13-007)

  • Claus Lamm

Austrian Science Fund (FWF P 32686)

  • Markus Rütgen
  • Claus Lamm

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Muireann Irish, University of Sydney, Australia

Ethics

Human subjects: Informed consent was obtained from all participants. For those participants whose images are to be published in eLife, consent to publish was obtained from each of them. More details can be found in Materials and Methods.The study was approved by the ethics committee of the Medical University of Vienna and was conducted in line with the latest version of the Declaration of Helsinki (2013).

Version history

  1. Received: May 3, 2021
  2. Preprint posted: May 20, 2021 (view preprint)
  3. Accepted: August 17, 2021
  4. Accepted Manuscript published: August 19, 2021 (version 1)
  5. Version of Record published: September 15, 2021 (version 2)

Copyright

© 2021, Zhao 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. Yili Zhao
  2. Lei Zhang
  3. Markus Rütgen
  4. Ronald Sladky
  5. Claus Lamm
(2021)
Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain
eLife 10:e69994.
https://doi.org/10.7554/eLife.69994

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https://doi.org/10.7554/eLife.69994

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