Broca area homologue's asymmetry reflects gestural communication lateralisation in monkeys (Papio anubis)
- CNRS, Aix-Marseille University, France
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
Konstantina Margiotoudi
Adrien Meguerditchian
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.
Reviewing Editor
- Timothy E Behrens, University of Oxford, United Kingdom
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.
Version history
- Preprint posted: February 9, 2021 (view preprint)
- Received: May 19, 2021
- Accepted: February 1, 2022
- Accepted Manuscript published: February 2, 2022 (version 1)
- 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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Broca area homologue's asymmetry reflects gestural communication lateralisation in monkeys (Papio anubis)
eLife 11:e70521.
https://doi.org/10.7554/eLife.70521
Further reading
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Asymmetries in the size of structures deep below the cortex explain how alpha oscillations in the brain respond to shifts in attention.
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Evidence suggests that subcortical structures play a role in high-level cognitive functions such as the allocation of spatial attention. While there is abundant evidence in humans for posterior alpha band oscillations being modulated by spatial attention, little is known about how subcortical regions contribute to these oscillatory modulations, particularly under varying conditions of cognitive challenge. In this study, we combined MEG and structural MRI data to investigate the role of subcortical structures in controlling the allocation of attentional resources by employing a cued spatial attention paradigm with varying levels of perceptual load. We asked whether hemispheric lateralization of volumetric measures of the thalamus and basal ganglia predicted the hemispheric modulation of alpha-band power. Lateral asymmetry of the globus pallidus, caudate nucleus, and thalamus predicted attention-related modulations of posterior alpha oscillations. When the perceptual load was applied to the target and the distractor was salient caudate nucleus asymmetry predicted alpha-band modulations. Globus pallidus was predictive of alpha-band modulations when either the target had a high load, or the distractor was salient, but not both. Finally, the asymmetry of the thalamus predicted alpha band modulation when neither component of the task was perceptually demanding. In addition to delivering new insight into the subcortical circuity controlling alpha oscillations with spatial attention, our finding might also have clinical applications. We provide a framework that could be followed for detecting how structural changes in subcortical regions that are associated with neurological disorders can be reflected in the modulation of oscillatory brain activity.
