Abstract

Witnessing another person's suffering elicits vicarious brain activity in areas active when we ourselves are in pain. Whether this activity influences prosocial behavior remains debated. Here participants witnessed a confederate express pain via a reaction of the swatted hand or via a facial expression and could decide to reduce that pain by donating money. Participants donate more money on trials in which the confederate expressed more pain. EEG shows that activity of the SI hand region explains variance in donation; TMS shows that altering this activity interferes with the pain-donation coupling only when pain is expressed by the hand and HD-tDCS that altering SI activity also interferes with pain perception. These experiments show vicarious somatosensory activations contribute to prosocial decision-making and suggest they do so by helping transform observed reactions of affected body-parts into accurate perceptions of pain that are necessary for decision making.

Data availability

fMRI and EEG data have been deposited in Zenodo. Source data files have been provided for all figures

The following data sets were generated

Article and author information

Author details

  1. Selene Gallo

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  2. Riccardo Paracampo

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

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Mario Carlo Severo

    Social Brain Lab, 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:" 0000-0001-7403-819X
  5. Laila Blömer

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Carolina Fernandes-Henriques

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  7. Anna Henschel

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  8. Balint Kalista Lammes

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  9. Tatjana Maskaljunas

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  10. Judith Suttrup

    Social Brain Lab, 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:" 0000-0002-4034-1534
  11. Alessio Avenanti

    Department of Psychology, University of Bologna, Bologna, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1139-9996
  12. Christian Keysers

    Social Brain Lab, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  13. 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 (VIDI: 452-14-015)

  • Valeria Gazzola

Brain and Behavior Research Foundation (NARSAD young investigator 22453)

  • Valeria Gazzola

H2020 European Research Council (ERC-StG-312511)

  • Christian Keysers

Cogito Foundation (R-117/13)

  • Alessio Avenanti

Fundação Bial (298/16)

  • Alessio Avenanti

Cogito Foundation (14-139-R)

  • Alessio Avenanti

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

Ethics

Human subjects: All studies have been approved by the Ethics Committee of the University of Amsterdam, the Netherlands.Project identifiers:2016-BC-73942016-BC-71302016-PSY-64852014-EXT-34762014-EXT-3432All participants received monetary compensation and gave their informed consent for participation in the study.

Reviewing Editor

  1. Peggy Mason, University of Chicago, United States

Version history

  1. Received: October 12, 2017
  2. Accepted: April 20, 2018
  3. Accepted Manuscript published: May 8, 2018 (version 1)
  4. Version of Record published: May 29, 2018 (version 2)

Copyright

© 2018, Gallo 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.

Metrics

  • 4,895
    Page views
  • 668
    Downloads
  • 49
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Selene Gallo
  2. Riccardo Paracampo
  3. Laura Müller-Pinzler
  4. Mario Carlo Severo
  5. Laila Blömer
  6. Carolina Fernandes-Henriques
  7. Anna Henschel
  8. Balint Kalista Lammes
  9. Tatjana Maskaljunas
  10. Judith Suttrup
  11. Alessio Avenanti
  12. Christian Keysers
  13. Valeria Gazzola
(2018)
The causal role of the somatosensory cortex in prosocial behaviour
eLife 7:e32740.
https://doi.org/10.7554/eLife.32740

Further reading

    1. Neuroscience
    Max L Sterling, Ruben Teunisse, Bernhard Englitz
    Tools and Resources Updated

    Ultrasonic vocalizations (USVs) fulfill an important role in communication and navigation in many species. Because of their social and affective significance, rodent USVs are increasingly used as a behavioral measure in neurodevelopmental and neurolinguistic research. Reliably attributing USVs to their emitter during close interactions has emerged as a difficult, key challenge. If addressed, all subsequent analyses gain substantial confidence. We present a hybrid ultrasonic tracking system, Hybrid Vocalization Localizer (HyVL), that synergistically integrates a high-resolution acoustic camera with high-quality ultrasonic microphones. HyVL is the first to achieve millimeter precision (~3.4–4.8 mm, 91% assigned) in localizing USVs, ~3× better than other systems, approaching the physical limits (mouse snout ~10 mm). We analyze mouse courtship interactions and demonstrate that males and females vocalize in starkly different relative spatial positions, and that the fraction of female vocalizations has likely been overestimated previously due to imprecise localization. Further, we find that when two male mice interact with one female, one of the males takes a dominant role in the interaction both in terms of the vocalization rate and the location relative to the female. HyVL substantially improves the precision with which social communication between rodents can be studied. It is also affordable, open-source, easy to set up, can be integrated with existing setups, and reduces the required number of experiments and animals.

    1. Neuroscience
    Federico G Segala, Aurelio Bruno ... Daniel H Baker
    Research Article

    How does the human brain combine information across the eyes? It has been known for many years that cortical normalization mechanisms implement ‘ocularity invariance’: equalizing neural responses to spatial patterns presented either monocularly or binocularly. Here, we used a novel combination of electrophysiology, psychophysics, pupillometry, and computational modeling to ask whether this invariance also holds for flickering luminance stimuli with no spatial contrast. We find dramatic violations of ocularity invariance for these stimuli, both in the cortex and also in the subcortical pathways that govern pupil diameter. Specifically, we find substantial binocular facilitation in both pathways with the effect being strongest in the cortex. Near-linear binocular additivity (instead of ocularity invariance) was also found using a perceptual luminance matching task. Ocularity invariance is, therefore, not a ubiquitous feature of visual processing, and the brain appears to repurpose a generic normalization algorithm for different visual functions by adjusting the amount of interocular suppression.