Empathic pain evoked by sensory and emotional-communicative cues share common and process-specific neural representation

  1. Feng Zhou  Is a corresponding author
  2. Jialin Li
  3. Weihua Zhao
  4. Lei Xu
  5. Xiaoxiao Zheng
  6. Meina Fu
  7. Shuxia Yao
  8. Keith M Kendrick
  9. Tor D Wager
  10. Benjamin Becker  Is a corresponding author
  1. University of Electronic Science and Technology of China, China
  2. Dartmouth College, United States

Abstract

Pain empathy can be evoked by multiple cues, particularly observation of acute pain inflictions or facial expressions of pain. Previous studies suggest that these cues commonly activate the insula and anterior cingulate, yet vicarious pain encompass pain-specific responses as well as unspecific processes (e.g., arousal) and overlapping activations are not sufficient to determine process-specific shared neural representations. We employed multivariate pattern analyses to fMRI data acquired during observation of noxious stimulation of body limbs (NS) and painful facial expressions (FE) and found spatially and functionally similar cross-modality (NS versus FE) whole-brain vicarious pain-predictive patterns. Further analyses consistently identified shared neural representations in the bilateral mid-insula. The vicarious pain patterns were not sensitive to respond to non-painful high-arousal negative stimuli but predicted self-experienced thermal pain. Finally, a domain-general vicarious pain pattern predictive of self-experienced pain but not arousal was developed. Our findings demonstrate shared pain-associated neural representations of vicarious pain.

Data availability

The functional MRI, numerical data as well as the Matlab scripts used to generate the figures have been deposited on the figshare repository under accession code 11994498 (https://figshare.com/articles/Vicarious_pain_dataset/11994498)Statistical and pattern weight maps are available on the Neurovault repository under collection 6332 (https://neurovault.org/collections/6332/). Statistical and pattern weight images are available on Neurovault

The following data sets were generated

Article and author information

Author details

  1. Feng Zhou

    Clinical Hospital of Chengdu Brain Science Institute, University of Electronic Science and Technology of China, Chengdu, China
    For correspondence
    zhou.feng@live.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Jialin Li

    Clinical Hospital of Chengdu Brain Science Institute, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Weihua Zhao

    Clinical Hospital of Chengdu Brain Science Institute, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Lei Xu

    Clinical Hospital of Chengdu Brain Science Institute, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Xiaoxiao Zheng

    Clinical Hospital of Chengdu Brain Science Institute, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Meina Fu

    Clinical Hospital of Chengdu Brain Science Institute, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Shuxia Yao

    Clinical Hospital of Chengdu Brain Science Institute, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Keith M Kendrick

    Key Laboratory for Neuroinformation of the Ministry of Education, School of Life Science and Technology, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0371-5904
  9. Tor D Wager

    Psychological & Brain Sciences, Dartmouth College, Hanover, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Benjamin Becker

    Clinical Hospital of Chengdu Brain Science Institute, University of Electronic Science and Technology of China, Chengdu, China
    For correspondence
    ben_becker@gmx.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9014-9671

Funding

National Natural Science Foundation of China (91632117)

  • Benjamin Becker

National Natural Science Foundation of China (31700998)

  • Keith M Kendrick

National Natural Science Foundation of China (31530032)

  • Shuxia Yao

National Institute of Mental Health (R01 MH116026)

  • Tor D Wager

National Institute of Biomedical Imaging and Bioengineering (R01EB026549)

  • Tor D Wager

National Key Research and Development Program of China (2018YFA0701400)

  • Benjamin Becker

Fundamental Research Funds for Central Universities (ZYGX2015Z002)

  • Benjamin Becker

Science, Innovation and Technology Department of the Sichuan Province (2018JY0001)

  • Benjamin Becker

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

Reviewing Editor

  1. Alexander Shackman, University of Maryland, United States

Ethics

Human subjects: All participants provided written informed consent for study participation and consent to publish the data. The study and all procedures were approved by the local ethics committee at the University of Electronic Science and Technology of China (Approval ID: 298) and was in accordance with the most recent revision of the Declaration of Helsinki.

Version history

  1. Received: March 14, 2020
  2. Accepted: September 5, 2020
  3. Accepted Manuscript published: September 7, 2020 (version 1)
  4. Version of Record published: September 21, 2020 (version 2)

Copyright

© 2020, Zhou 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. Feng Zhou
  2. Jialin Li
  3. Weihua Zhao
  4. Lei Xu
  5. Xiaoxiao Zheng
  6. Meina Fu
  7. Shuxia Yao
  8. Keith M Kendrick
  9. Tor D Wager
  10. Benjamin Becker
(2020)
Empathic pain evoked by sensory and emotional-communicative cues share common and process-specific neural representation
eLife 9:e56929.
https://doi.org/10.7554/eLife.56929

Share this article

https://doi.org/10.7554/eLife.56929

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