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Agent-based representations of objects and actions in the monkey pre-supplementary motor area

Alessandro Livi, Marco Lanzilotto, Monica Maranesi, Leonardo Fogassi, Giacomo Rizzolatti, and Luca Bonini
PNAS February 12, 2019 116 (7) 2691-2700; published ahead of print February 12, 2019 https://doi.org/10.1073/pnas.1810890116
Alessandro Livi
aDepartment of Medicine and Surgery, Neuroscience Unit, University of Parma, 43125 Parma, Italy;
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  • For correspondence: alessandro.livi2@gmail.comgiacomo.rizzolatti@unipr.itluca.bonini@unipr.it
Marco Lanzilotto
aDepartment of Medicine and Surgery, Neuroscience Unit, University of Parma, 43125 Parma, Italy;
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  • ORCID record for Marco Lanzilotto
Monica Maranesi
aDepartment of Medicine and Surgery, Neuroscience Unit, University of Parma, 43125 Parma, Italy;
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Leonardo Fogassi
aDepartment of Medicine and Surgery, Neuroscience Unit, University of Parma, 43125 Parma, Italy;
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Giacomo Rizzolatti
aDepartment of Medicine and Surgery, Neuroscience Unit, University of Parma, 43125 Parma, Italy;bParma Unit, Institute of Neuroscience of Centro Nazionale delle Ricerche (CNR), 43125 Parma, Italy
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  • For correspondence: alessandro.livi2@gmail.comgiacomo.rizzolatti@unipr.itluca.bonini@unipr.it
Luca Bonini
aDepartment of Medicine and Surgery, Neuroscience Unit, University of Parma, 43125 Parma, Italy;
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  • For correspondence: alessandro.livi2@gmail.comgiacomo.rizzolatti@unipr.itluca.bonini@unipr.it
  1. Contributed by Giacomo Rizzolatti, December 7, 2018 (sent for review July 2, 2018; reviewed by Atsushi Iriki and Roger N. Lemon)

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Significance

Social animals exploit information about objects for planning actions and for predicting those of others. Here, we show that pre-supplementary motor area F6 hosts different types of neurons responding to visually presented objects when they are targeted by the monkey’s own action (self-type), another agent’s action (other-type), or both (self- and other-type). These findings suggest the existence in area F6 of an “object-mirroring” mechanism, which allows observers to predict others’ impending action by recruiting the same motor representation they would use for planning their own action in the same context, before the activation of classical “action-mirroring” mechanisms.

Abstract

Information about objects around us is essential for planning actions and for predicting those of others. Here, we studied pre-supplementary motor area F6 neurons with a task in which monkeys viewed and grasped (or refrained from grasping) objects, and then observed a human doing the same task. We found “action-related neurons” encoding selectively monkey’s own action [self-type (ST)], another agent’s action [other-type (OT)], or both [self- and other-type (SOT)]. Interestingly, we found “object-related neurons” exhibiting the same type of selectivity before action onset: Indeed, distinct sets of neurons discharged when visually presented objects were targeted by the monkey’s own action (ST), another agent’s action (OT), or both (SOT). Notably, object-related neurons appear to signal self and other’s intention to grasp and the most likely grip type that will be performed, whereas action-related neurons encode a general goal attainment signal devoid of any specificity for the observed grip type. Time-resolved cross-modal population decoding revealed that F6 neurons first integrate information about object and context to generate an agent-shared signal specifying whether and how the object will be grasped, which progressively turns into a broader agent-based goal attainment signal during action unfolding. Importantly, shared representation of objects critically depends upon their location in the observer’s peripersonal space, suggesting an “object-mirroring” mechanism through which observers could accurately predict others’ impending action by recruiting the same motor representation they would activate if they were to act upon the same object in the same context.

  • mirror neuron
  • macaque
  • object processing
  • action prediction
  • pre-SMA

Footnotes

  • ↵1A.L. and M.L. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: alessandro.livi2{at}gmail.com, giacomo.rizzolatti{at}unipr.it, or luca.bonini{at}unipr.it.
  • ↵3Present address: Department of Neuroscience, Washington University, St. Louis, MO 63130.

  • Author contributions: G.R. and L.B. designed research; A.L., M.L., and L.B. performed research; A.L., M.L., and M.M. analyzed data; and A.L., M.L., L.F., G.R., and L.B. wrote the paper.

  • Reviewers: A.I., RIKEN Center for Biosystems Dynamics Research; and R.N.L., University College London.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1810890116/-/DCSupplemental.

  • Copyright © 2019 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).

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Agent-based representations of objects and actions in the monkey pre-supplementary motor area
Alessandro Livi, Marco Lanzilotto, Monica Maranesi, Leonardo Fogassi, Giacomo Rizzolatti, Luca Bonini
Proceedings of the National Academy of Sciences Feb 2019, 116 (7) 2691-2700; DOI: 10.1073/pnas.1810890116

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Agent-based representations of objects and actions in the monkey pre-supplementary motor area
Alessandro Livi, Marco Lanzilotto, Monica Maranesi, Leonardo Fogassi, Giacomo Rizzolatti, Luca Bonini
Proceedings of the National Academy of Sciences Feb 2019, 116 (7) 2691-2700; DOI: 10.1073/pnas.1810890116
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