1. Neuroscience

Non-shared coding of observed and executed actions prevails in macaque ventral premotor mirror neurons

  1. Jörn K Pomper  Is a corresponding author
  2. Mohammad Shams
  3. Shengjun Wen
  4. Friedemann Bunjes
  5. Peter Thier
  1. University of Tübingen, Germany
https://doi.org/10.7554/eLife.77513
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  1. Jörn K Pomper
  2. Mohammad Shams
  3. Shengjun Wen
  4. Friedemann Bunjes
  5. Peter Thier
(2023)
Non-shared coding of observed and executed actions prevails in macaque ventral premotor mirror neurons
eLife 12:e77513.
https://doi.org/10.7554/eLife.77513
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Abstract

According to the mirror mechanism the discharge of F5 mirror neurons of a monkey observing another individual performing an action is a motor representation of the observed action that may serve to understand or learn from the action. This hypothesis, if strictly interpreted, requires mirror neurons to exhibit an action tuning that is shared between action observation and execution. Due to insufficient data it remains contentious if this requirement is met. To fill in the gaps, we conducted an experiment in which identical objects had to be manipulated in three different ways in order to serve distinct action goals. Using three methods, including cross-task classification, we found that at most time points F5 mirror neurons did not encode observed actions with the same code underlying action execution. However, in about 20% of neurons there were time periods with a shared code. These time periods formed a distinct cluster and cannot be considered a product of chance. Population classification yielded non-shared coding for observed actions in the whole population, which was at times optimal and consistently better than shared coding in differentially selected subpopulations. These results support the hypothesis of a representation of observed actions based on a strictly defined mirror mechanism only for small subsets of neurons and only under the assumption of time-resolved readout. Considering alternative concepts and recent findings, we propose that during observation mirror neurons represent the process of a goal pursuit from the observer's viewpoint. Whether the observer's goal pursuit, in which the other's action goal becomes the observer's action goal, or the other's goal pursuit is represented remains to be clarified. In any case, it may allow the observer to use expectations associated with a goal pursuit to directly intervene in or learn from another's action.

Data availability

The data and codes for reproduction of all figures and the table have been deposited on Zenodo. During the review process, they are made available to the reviewers/editors. After acceptance, they are freely accessible.

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Author details

  1. Jörn K Pomper

    Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    For correspondence
    joern.pomper@uni-tuebingen.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0926-0477

  2. Mohammad Shams

    Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5081-3427

  3. Shengjun Wen

    Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  4. Friedemann Bunjes

    Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  5. Peter Thier

    Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5909-4222

Funding

Deutsche Forschungsgemeinschaft (TH 425/12-2)

  • Jörn K Pomper
  • Mohammad Shams
  • Shengjun Wen
  • Friedemann Bunjes
  • Peter Thier

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

Ethics

Animal experimentation: All experiments were approved and controlled by the regional veterinary administration (Regierungspräsidium Tübingen and Landratsamt Tübingen, Permit Number: N4/14) and conducted in accordance with German and European law and the National Institutes of Health's Guide for the Care and Use of Laboratory Animals, and regularly and carefully monitored by the veterinary service of the University of Tübingen, the latter also providing care in case of medical problems.

Copyright

© 2023, Pomper 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. Jörn K Pomper
  2. Mohammad Shams
  3. Shengjun Wen
  4. Friedemann Bunjes
  5. Peter Thier
(2023)
Non-shared coding of observed and executed actions prevails in macaque ventral premotor mirror neurons
eLife 12:e77513.
https://doi.org/10.7554/eLife.77513

Share this article

https://doi.org/10.7554/eLife.77513

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