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

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.

The following data sets were generated

Article and author information

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.

Reviewing Editor

  1. Kristine Krug, Otto-von-Guericke University Magdeburg, Germany

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.

Version history

  1. Received: February 2, 2022
  2. Preprint posted: February 4, 2022 (view preprint)
  3. Accepted: July 14, 2023
  4. Accepted Manuscript published: July 17, 2023 (version 1)
  5. Version of Record published: August 9, 2023 (version 2)

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.

Metrics

  • 598
    views
  • 126
    downloads
  • 2
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. 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

Further reading

    1. Biochemistry and Chemical Biology
    2. Neuroscience
    Maximilian Nagel, Marco Niestroj ... Marc Spehr
    Research Article

    In most mammals, conspecific chemosensory communication relies on semiochemical release within complex bodily secretions and subsequent stimulus detection by the vomeronasal organ (VNO). Urine, a rich source of ethologically relevant chemosignals, conveys detailed information about sex, social hierarchy, health, and reproductive state, which becomes accessible to a conspecific via vomeronasal sampling. So far, however, numerous aspects of social chemosignaling along the vomeronasal pathway remain unclear. Moreover, since virtually all research on vomeronasal physiology is based on secretions derived from inbred laboratory mice, it remains uncertain whether such stimuli provide a true representation of potentially more relevant cues found in the wild. Here, we combine a robust low-noise VNO activity assay with comparative molecular profiling of sex- and strain-specific mouse urine samples from two inbred laboratory strains as well as from wild mice. With comprehensive molecular portraits of these secretions, VNO activity analysis now enables us to (i) assess whether and, if so, how much sex/strain-selective ‘raw’ chemical information in urine is accessible via vomeronasal sampling; (ii) identify which chemicals exhibit sufficient discriminatory power to signal an animal’s sex, strain, or both; (iii) determine the extent to which wild mouse secretions are unique; and (iv) analyze whether vomeronasal response profiles differ between strains. We report both sex- and, in particular, strain-selective VNO representations of chemical information. Within the urinary ‘secretome’, both volatile compounds and proteins exhibit sufficient discriminative power to provide sex- and strain-specific molecular fingerprints. While total protein amount is substantially enriched in male urine, females secrete a larger variety at overall comparatively low concentrations. Surprisingly, the molecular spectrum of wild mouse urine does not dramatically exceed that of inbred strains. Finally, vomeronasal response profiles differ between C57BL/6 and BALB/c animals, with particularly disparate representations of female semiochemicals.

    1. Neuroscience
    Kenta Abe, Yuki Kambe ... Tatsuo Sato
    Research Article

    Midbrain dopamine neurons impact neural processing in the prefrontal cortex (PFC) through mesocortical projections. However, the signals conveyed by dopamine projections to the PFC remain unclear, particularly at the single-axon level. Here, we investigated dopaminergic axonal activity in the medial PFC (mPFC) during reward and aversive processing. By optimizing microprism-mediated two-photon calcium imaging of dopamine axon terminals, we found diverse activity in dopamine axons responsive to both reward and aversive stimuli. Some axons exhibited a preference for reward, while others favored aversive stimuli, and there was a strong bias for the latter at the population level. Long-term longitudinal imaging revealed that the preference was maintained in reward- and aversive-preferring axons throughout classical conditioning in which rewarding and aversive stimuli were paired with preceding auditory cues. However, as mice learned to discriminate reward or aversive cues, a cue activity preference gradually developed only in aversive-preferring axons. We inferred the trial-by-trial cue discrimination based on machine learning using anticipatory licking or facial expressions, and found that successful discrimination was accompanied by sharper selectivity for the aversive cue in aversive-preferring axons. Our findings indicate that a group of mesocortical dopamine axons encodes aversive-related signals, which are modulated by both classical conditioning across days and trial-by-trial discrimination within a day.