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

F5 mirror neurons action selection goal pursuit mirror mechanism neuroscience premotor cortex rhesus macaque social learning

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
17 07 2023
Historique:
received: 02 02 2022
accepted: 14 07 2023
medline: 10 8 2023
pubmed: 17 7 2023
entrez: 17 7 2023
Statut: epublish

Résumé

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.

Identifiants

pubmed: 37458338
doi: 10.7554/eLife.77513
pii: 77513
pmc: PMC10411969
doi:
pii:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023, Pomper, Shams, Wen et al.

Déclaration de conflit d'intérêts

JP, MS, SW, FB, PT No competing interests declared

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Auteurs

Jörn K Pomper (JK)

Cognitive Neurology Laboratory, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
Department of Neurology & Stroke, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

Mohammad Shams (M)

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

Shengjun Wen (S)

Cognitive Neurology Laboratory, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
Graduate Training Centre of Neuroscience, International Max Planck Research School, University of Tübingen, 72076 , Germany, Tübingen, Germany.

Friedemann Bunjes (F)

Cognitive Neurology Laboratory, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

Peter Thier (P)

Cognitive Neurology Laboratory, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

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Classifications MeSH