Human larynx motor cortices coordinate respiration for vocal-motor control

Vocal flexibility is a hallmark of the human species, most particularly the capacity to speak and sing. This ability is supported in part by the evolution of a direct neural pathway linking the motor cortex to the brainstem nucleus that controls the larynx the primary sound source for communication....

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Main Authors: Michel Belyk, Rachel Brown, Deryk S. Beal, Alard Roebroeck, Carolyn McGettigan, Stella Guldner, Sonja A. Kotz
Format: Article
Language:English
Published: Elsevier 2021-10-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811921006029
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author Michel Belyk
Rachel Brown
Deryk S. Beal
Alard Roebroeck
Carolyn McGettigan
Stella Guldner
Sonja A. Kotz
author_facet Michel Belyk
Rachel Brown
Deryk S. Beal
Alard Roebroeck
Carolyn McGettigan
Stella Guldner
Sonja A. Kotz
author_sort Michel Belyk
collection DOAJ
description Vocal flexibility is a hallmark of the human species, most particularly the capacity to speak and sing. This ability is supported in part by the evolution of a direct neural pathway linking the motor cortex to the brainstem nucleus that controls the larynx the primary sound source for communication. Early brain imaging studies demonstrated that larynx motor cortex at the dorsal end of the orofacial division of motor cortex (dLMC) integrated laryngeal and respiratory control, thereby coordinating two major muscular systems that are necessary for vocalization. Neurosurgical studies have since demonstrated the existence of a second larynx motor area at the ventral extent of the orofacial motor division (vLMC) of motor cortex. The vLMC has been presumed to be less relevant to speech motor control, but its functional role remains unknown. We employed a novel ultra-high field (7T) magnetic resonance imaging paradigm that combined singing and whistling simple melodies to localise the larynx motor cortices and test their involvement in respiratory motor control. Surprisingly, whistling activated both ‘larynx areas’ more strongly than singing despite the reduced involvement of the larynx during whistling. We provide further evidence for the existence of two larynx motor areas in the human brain, and the first evidence that laryngeal-respiratory integration is a shared property of both larynx motor areas. We outline explicit predictions about the descending motor pathways that give these cortical areas access to both the laryngeal and respiratory systems and discuss the implications for the evolution of speech.
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spelling doaj.art-1c594b2424ec4eb582a6f002a14cc4572022-12-21T23:34:01ZengElsevierNeuroImage1095-95722021-10-01239118326Human larynx motor cortices coordinate respiration for vocal-motor controlMichel Belyk0Rachel Brown1Deryk S. Beal2Alard Roebroeck3Carolyn McGettigan4Stella Guldner5Sonja A. Kotz6Department of Speech Hearing and Phonetic Sciences, University College London, London, United KingdomFaculty of Psychology and Neuroscience, University of Maastricht, Maastricht, The Netherlands; RWTH Aachen University, Institute for Psychology, Aachen GermanyBloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, Ontario, Canada; Department of Speech-Language Pathology, University of Toronto, Toronto, Ontario, CanadaFaculty of Psychology and Neuroscience, University of Maastricht, Maastricht, The NetherlandsDepartment of Speech Hearing and Phonetic Sciences, University College London, London, United KingdomDepartment of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, GermanyFaculty of Psychology and Neuroscience, University of Maastricht, Maastricht, The Netherlands; Department of Neuropsychology, Max Planck Institute for Human and Cognitive Sciences, Leipzig, Germany; Corresponding author.Vocal flexibility is a hallmark of the human species, most particularly the capacity to speak and sing. This ability is supported in part by the evolution of a direct neural pathway linking the motor cortex to the brainstem nucleus that controls the larynx the primary sound source for communication. Early brain imaging studies demonstrated that larynx motor cortex at the dorsal end of the orofacial division of motor cortex (dLMC) integrated laryngeal and respiratory control, thereby coordinating two major muscular systems that are necessary for vocalization. Neurosurgical studies have since demonstrated the existence of a second larynx motor area at the ventral extent of the orofacial motor division (vLMC) of motor cortex. The vLMC has been presumed to be less relevant to speech motor control, but its functional role remains unknown. We employed a novel ultra-high field (7T) magnetic resonance imaging paradigm that combined singing and whistling simple melodies to localise the larynx motor cortices and test their involvement in respiratory motor control. Surprisingly, whistling activated both ‘larynx areas’ more strongly than singing despite the reduced involvement of the larynx during whistling. We provide further evidence for the existence of two larynx motor areas in the human brain, and the first evidence that laryngeal-respiratory integration is a shared property of both larynx motor areas. We outline explicit predictions about the descending motor pathways that give these cortical areas access to both the laryngeal and respiratory systems and discuss the implications for the evolution of speech.http://www.sciencedirect.com/science/article/pii/S1053811921006029VoiceRespirationLarynxMotor cortexfMRISong
spellingShingle Michel Belyk
Rachel Brown
Deryk S. Beal
Alard Roebroeck
Carolyn McGettigan
Stella Guldner
Sonja A. Kotz
Human larynx motor cortices coordinate respiration for vocal-motor control
NeuroImage
Voice
Respiration
Larynx
Motor cortex
fMRI
Song
title Human larynx motor cortices coordinate respiration for vocal-motor control
title_full Human larynx motor cortices coordinate respiration for vocal-motor control
title_fullStr Human larynx motor cortices coordinate respiration for vocal-motor control
title_full_unstemmed Human larynx motor cortices coordinate respiration for vocal-motor control
title_short Human larynx motor cortices coordinate respiration for vocal-motor control
title_sort human larynx motor cortices coordinate respiration for vocal motor control
topic Voice
Respiration
Larynx
Motor cortex
fMRI
Song
url http://www.sciencedirect.com/science/article/pii/S1053811921006029
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