Auditory representation of learned sound sequences in motor regions of the macaque brain.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
30 06 2020
Historique:
pubmed: 17 6 2020
medline: 2 9 2020
entrez: 17 6 2020
Statut: ppublish

Résumé

Human speech production requires the ability to couple motor actions with their auditory consequences. Nonhuman primates might not have speech because they lack this ability. To address this question, we trained macaques to perform an auditory-motor task producing sound sequences via hand presses on a newly designed device ("monkey piano"). Catch trials were interspersed to ascertain the monkeys were listening to the sounds they produced. Functional MRI was then used to map brain activity while the animals listened attentively to the sound sequences they had learned to produce and to two control sequences, which were either completely unfamiliar or familiar through passive exposure only. All sounds activated auditory midbrain and cortex, but listening to the sequences that were learned by self-production additionally activated the putamen and the hand and arm regions of motor cortex. These results indicate that, in principle, monkeys are capable of forming internal models linking sound perception and production in motor regions of the brain, so this ability is not special to speech in humans. However, the coupling of sounds and actions in nonhuman primates (and the availability of an internal model supporting it) seems not to extend to the upper vocal tract, that is, the supralaryngeal articulators, which are key for the production of speech sounds in humans. The origin of speech may have required the evolution of a "command apparatus" similar to the control of the hand, which was crucial for the evolution of tool use.

Identifiants

pubmed: 32541016
pii: 1915610117
doi: 10.1073/pnas.1915610117
pmc: PMC7334521
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

15242-15252

Subventions

Organisme : NIDCD NIH HHS
ID : R01 DC014989
Pays : United States

Informations de copyright

Copyright © 2020 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

The authors declare no competing interest.

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Auteurs

Denis Archakov (D)

Department of Neuroscience, Georgetown University Medical Center, Washington, DC 20057.
Brain and Mind Laboratory, Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, FI-02150 Espoo, Finland.

Iain DeWitt (I)

Department of Neuroscience, Georgetown University Medical Center, Washington, DC 20057.

Paweł Kuśmierek (P)

Department of Neuroscience, Georgetown University Medical Center, Washington, DC 20057.

Michael Ortiz-Rios (M)

Department of Neuroscience, Georgetown University Medical Center, Washington, DC 20057.

Daniel Cameron (D)

Department of Neuroscience, Georgetown University Medical Center, Washington, DC 20057.

Ding Cui (D)

Department of Neuroscience, Georgetown University Medical Center, Washington, DC 20057.

Elyse L Morin (EL)

Department of Neuroscience, Georgetown University Medical Center, Washington, DC 20057.

John W VanMeter (JW)

Center for Functional and Molecular Imaging, Georgetown University Medical Center, Washington, DC 20057.

Mikko Sams (M)

Brain and Mind Laboratory, Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, FI-02150 Espoo, Finland.

Iiro P Jääskeläinen (IP)

Brain and Mind Laboratory, Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, FI-02150 Espoo, Finland.

Josef P Rauschecker (JP)

Department of Neuroscience, Georgetown University Medical Center, Washington, DC 20057; rauschej@georgetown.edu.

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