Human larynx motor cortices coordinate respiration for vocal-motor control

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 studies demonstrated that a larynx motor area 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. This dual motor representation of the larynx is notably unique to humans, though it is not known what these two larynx motor areas contribute separately to voice motor control. We localized the dorsal and ventral larynx motor cortices by having participants sing worldess melodies while undergoing ultra-high field magnetic resonance imaging and tested the involvement of respiratory motor control in the same regions by having participants whistle simple melodies. Surprisingly, both singing and whistling increased activation of both larynx areas despite the lack of involvement of the larynx during whistling. These findings demonstrate that both larynx-controlling regions participate in respiratory motor control in addition to laryngeal motor control, since singing and whistling share exhalation as a common source of mechanical power for sound production. The integration of laryngeal and respiratory motor control may be an adaptation that has supported the evolution of speech in humans.

Speech-Driven Spectrotemporal Receptive Fields Beyond the Auditory Cortex

“…We have independently suggested that dPM is part of the cortical circuit for laryngeal motor control (Hickok, 2017). Therefore, one hypothesis is that dPM responds to multiple aspects of speech motor control during production (Belyk et al, 2020;Cheung et al, 2016) but responds preferentially to pitch/voicing during perception (Cheung et al, 2016), which may owe to the presence of non-identical subpopulations of neurons coding auditory and motor features, respectively, as is typical of brain regions involved in sensorimotor integration (Sakata, Taira, Murata, & Mine, 1995).…”

Two cortical representations of voice control are differentially involved in speech fluency

“…Our vLMC seed co-ordinate was derived from the first dMRI study on stuttering ( x = −48, y = −15 and z = 18) ( Sommer et al , 2002 ). This white-matter site is closely located to sites of cortical activity reported for tasks that were designed to stimulate and differentiate dLMC and vLMC brain activity during whistling and singing ( x = −59, y = −16 and z = 13) ( Belyk et al ., 2020 ) or vocalization and vowel production ( x = −58, y = −2 and z = 20) ( Eichert et al ., 2020 ). Similarly, earlier fMRI studies that investigated vowel production ( Grabski et al , 2012 ), vocal imitation ( Belyk et al , 2016 ), pitch ( Peck et al , 2009 ), cough ( Mazzone et al , 2011 ) and brain alterations in spasmodic dysphonia ( Simonyan and Ludlow, 2012 ) relate laryngeal control to our chosen vLMC co-ordinate.…”

“…Similarly, earlier fMRI studies that investigated vowel production ( Grabski et al , 2012 ), vocal imitation ( Belyk et al , 2016 ), pitch ( Peck et al , 2009 ), cough ( Mazzone et al , 2011 ) and brain alterations in spasmodic dysphonia ( Simonyan and Ludlow, 2012 ) relate laryngeal control to our chosen vLMC co-ordinate. Cyto- and myeloarchitecture of the ventral laryngeal representation is currently unknown and it has been suggested that this region might belong to the cytoarchitectonic area 6 ( Pfenning et al , 2014 ; Dichter et al , 2018 ; Jarvis, 2019 ; Eichert et al ., 2020 ) or to the cytoarchitectonic area 43 ( Belyk and Brown, 2017 ; Belyk et al ., 2020 ). Besides this dissent, different research groups seem to agree on the idea that the vLMC does not belong to the primary motor cortex.…”

“…Deeper structures such as the sulcal regions of the pre-central gyrus are better accessible via magnetic resonance imaging (MRI) techniques. A recent ultra-high field functional MRI study tested the involvement of dLMC and vLMC neurons in respiratory motor control by having participants whistle and singing simple melodies ( Belyk et al ., 2020 ). Both LMC regions were involved during singing as well as whistling, suggesting their functional contribution to voicing and expiration.…”

“…This ventral extension of the central sulcus harbours the vLMC ( Foerster, 1936 ; Bouchard et al , 2013 ; Breshears et al , 2015 ). Only recently, studies have started targeting and differentiating findings from the dorsal and the ventral motor representation of voice control ( Dichter et al , 2018 ; Belyk et al ., 2020 ). Ultimately, fundamental questions exist about what is the structural organization of the vLMC network, does it differ from dLMC network organization and will the learning of a changed voicing behaviour reorganize the structural network formation within both networks?…”