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

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

doi:10.7554/eLife.77513

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

Elife. 2023 Jul 17:12:e77513. doi: 10.7554/eLife.77513.

Authors

Jörn K Pomper^#^{1

2}, Mohammad Shams^#^{1

3

4}, Shengjun Wen^#^{1

3}, Friedemann Bunjes¹, Peter Thier¹

Affiliations

¹ Cognitive Neurology Laboratory, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
² Department of Neurology & Stroke, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
³ Graduate Training Centre of Neuroscience, International Max Planck Research School, University of Tübingen, 72076 , Germany, Tübingen, Germany.
⁴ Department of Psychology, York University, Toronto, Canada.

^# Contributed equally.

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.

Keywords: F5 mirror neurons; action selection; goal pursuit; mirror mechanism; neuroscience; premotor cortex; rhesus macaque; social learning.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Action Potentials / physiology
Animals
Macaca
Mirror Neurons* / physiology
Motor Cortex* / physiology
Psychomotor Performance / physiology

Grants and funding

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