Broca area homologue's asymmetry reflects gestural communication lateralisation in monkeys (Papio anubis)

Abstract

Manual gestures and speech recruit a common neural network, involving Broca's area in the left hemisphere. Such speech-gesture integration gave rise to theories on the critical role of manual gesturing in the origin of language. Within this evolutionary framework, research on gestural communication in our closer primate relatives has received renewed attention for investigating its potential language-like features. Here, using in-vivo anatomical MRI in 50 baboons, we found that communicative gesturing is related to Broca homologue's marker in monkeys, namely the ventral portion of the Inferior Arcuate sulcus (IA sulcus). In fact, both direction and degree of gestural communication's handedness - but not handedness for object manipulation - are associated and correlated with contralateral depth asymmetry at this exact IA sulcus portion. In other words, baboons that prefer to communicate with their right hand have a deeper left-than-right IA sulcus, than those preferring to communicate with their left hand and vice versa. Interestingly, in contrast to handedness for object manipulation, gestural communication's lateralisation is not associated to the Central sulcus depth asymmetry, suggesting a double dissociation of handedness' types between manipulative action and gestural communication. It is thus not excluded that this specific gestural lateralisation signature within the baboons' frontal cortex might reflect a phylogenetical continuity with language-related Broca lateralisation in humans.

Data availability

The behavioural, neuro-anatomical and statistic code data that support the findings of this study are available in "OSF Storage" with the identifier DOI 10.17605/OSF.IO/DPXS5.https://osf.io/dpxs5/?view_only=f406ad972edd43e485e5e4076bae0f78

Article and author information

Author details

  1. Yannick Becker

    UMR7290, Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Nicolas Claidière

    UMR7290, Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Konstantina Margiotoudi

    UMR7290, Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9505-3978
  4. Damien Marie

    UMR7290, Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Muriel Roth

    Centre IRMf Institut de Neurosciences de la Timone, CNRS, Aix-Marseille University, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Bruno Nazarian

    Centre IRM Institut de Neurosciences de la Timone, CNRS, Aix-Marseille University, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Jean-Luc Anton

    Centre IRM Institut de Neurosciences de la Timone, CNRS, Aix-Marseille University, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Olivier Coulon

    Institut de Neurosciences de la Timone, CNRS, Aix-Marseille University, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Adrien Meguerditchian

    Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, Marseille, France
    For correspondence
    adrien.meguerditchian@univ-amu.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3754-6747

Funding

H2020 European Research Council (716931 - GESTIMAGE - ERC-2016-STG)

  • Adrien Meguerditchian

Agence Nationale de la Recherche (ANR-12-PDOC-0014-01)

  • Adrien Meguerditchian

Agence Nationale de la Recherche (ANR-16-CONV-0002)

  • Adrien Meguerditchian

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 baboons were housed in social groups at the Station de Primatologie CNRS (UPS 846, Rousset, France; Agreement number for conducting experiments on vertebrate animals: D13-087-7) and have free access to outdoor areas connected to indoor areas. Wooden and metallic, ethologically approved, structures enrich the enclosures. Feeding times are held four times a day with seeds, monkey pellets and fresh fruits and vegetables. Water is available ad libitum. The study was approved by the "C2EA-71 Ethical Committee of Neurosciences" (INT Marseille) under the number APAFIS#13553-201802151547729. The experimental procedure complied with the current French laws and the European directive 86/609/CEE.

Reviewing Editor

  1. Timothy E Behrens, University of Oxford, United Kingdom

Publication history

  1. Preprint posted: February 9, 2021 (view preprint)
  2. Received: May 19, 2021
  3. Accepted: February 1, 2022
  4. Accepted Manuscript published: February 2, 2022 (version 1)
  5. Version of Record published: February 15, 2022 (version 2)

Copyright

© 2022, Becker 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. Yannick Becker
  2. Nicolas Claidière
  3. Konstantina Margiotoudi
  4. Damien Marie
  5. Muriel Roth
  6. Bruno Nazarian
  7. Jean-Luc Anton
  8. Olivier Coulon
  9. Adrien Meguerditchian
(2022)
Broca area homologue's asymmetry reflects gestural communication lateralisation in monkeys (Papio anubis)
eLife 11:e70521.
https://doi.org/10.7554/eLife.70521

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