Human larynx motor cortices coordinate respiration for vocal-motor control

Michel Belyk,Rachel Brown,Deryk S Beal,Alard Roebroeck,Carolyn Mcgettigan,Stella Guldner,Sonja A Kotz

doi:10.1016/j.neuroimage.2021.118326

Abstract

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.

Highlights

Diverse and flexible vocal communication is a hallmark of the human species, most notably in the ability to speak and sing
We suggest that in addition to their established roles in laryngeal motor control, the dorsal Larynx Motor Cortex (dLMC) and ventral Larynx Motor Cortex (vLMC) contribute to respiratory motor control and may serve to integrate two muscular systems that require mutual coordination to support important behaviours such as speaking, singing, and airway protection
We suggest that neither the dLMC nor the vLMC are strictly laryngeal, and that both may integrate laryngeal and respiratory motor control

Summary

Introduction

Diverse and flexible vocal communication is a hallmark of the human species, most notably in the ability to speak and sing. Monkeys are weak vocal learners (Fischer and Hammerschmidt, 2019), while non-human apes appear to have intermediate VPL abilities (Lameira et al, 2016; Wich et al, 2012) as well as some facility in controlling the respiratory drive for sound production (Lameira et al, 2013; Perlman and Clark, 2015; Wich et al, 2009). These abilities are supported by specialisations in the motor system that have been considerably altered over course of primate evolution. The dorsal Larynx Motor Cortex (dLMC) is located deep within the central sulcus in primary motor cortex and is adjacent to articulatory motor regions for the lips and

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