Tongue acceleration in humans evoked with intramuscular electrical stimulation of genioglossus
Introduction
Movement of the tongue plays a critical role in breathing as the posterior part of the tongue forms the anterior wall of the pharynx in the upper airway. In healthy awake participants, the tongue moves anteriorly (≥ 1 mm) during inspiration (Brown et al., 2013; Cheng et al., 2008), dilating the upper airway to oppose the collapsing force from increased negative intraluminal pressure generated by the inspiratory muscles. The magnitude of anterior movement of the tongue is related to the size of the pharyngeal airway, increasing in people with narrow airways (e.g. due to obesity or craniofacial narrowing) but are otherwise healthy (Cheng et al., 2014). Minimal anterior movement (< 1 mm) of the tongue has also been observed in healthy participants (Jugé et al., 2020; see also Kwan et al., 2014), perhaps due to greater stiffening, than dilation, of the upper airway, as a means of protecting against collapse. Conversely, posterior movement of the tongue narrows the pharyngeal airway to increase collapsibility and contributes to the pathogenesis of obstructive sleep apnoea (OSA), a common condition characterised by episodes of narrowing or obstruction of the pharyngeal airway during sleep (Malhotra and White, 2002). Accordingly, the muscles that control the movement of the tongue have been a focus for potential treatments of OSA (Dotan et al., 2011; Oliven et al., 2003; Schwartz et al., 2014; Steier et al., 2011; Strohl et al., 2016).
The genioglossus is the most commonly studied muscle in OSA as it is the largest and most effective dilator muscle of the upper airway (Odeh et al., 1993; Schnall et al., 1995); sitting at the base of the tongue its main function is to depress and protrude the tongue. Several studies report that intramuscular electrical stimulation of genioglossus improves airflow and reduces upper airway resistance during flow-limited breaths in OSA (Oliven et al., 2003, 2001; Schwartz et al., 1996; Smith et al., 1996). However, studies investigating the direct effects of genioglossus stimulation on tongue movement have been limited, most likely due to the difficulties in instrumenting the upper airway. Both Schnall et al. (1995) and Oliven et al. (2001) indirectly show anterior movement of the tongue with non-invasive, sublingual stimulation of genioglossus through the increase in protrusion force generated against a balloon pressure transducer placed inside the mouth. Endoscopic assessment in both healthy awake participants (Mann et al., 2002) and people with OSA anaesthetised with propofol (Dotan et al., 2011) demonstrated that intramuscular electrical stimulation of genioglossus enlarges the anteroposterior diameter of the pharyngeal airway. The latter study by Dotan et al. (2011) is notable in that they stimulated the genioglossus non-concurrently at two separate sites, an anterior and posterior site, opposed to the single, non-specific sites used in previous studies which would have assumed that the muscle operated as a single functional unit. About this time, Mu and Sanders (2010) described two neuromuscular compartments for the genioglossus, a shallow, relative to the skin, horizontal compartment and a deeper oblique compartment, based on distinct fibre orientations and their innervation by separate branches of the medial branch of the hypoglossal nerve. Contraction of shallow, horizontal fibres is more conducive to anterior movement and protrusion of the tongue, whereas contraction of deep, oblique fibres is more suitable for depression of the tongue.
Tagged magnetic resonance imaging of the tongue during breathing has also revealed several distinct movement patterns for genioglossus (Brown et al., 2013; Cheng et al., 2008; Jugé et al., 2020). In Jugé et al. (2020), each movement pattern tended to involve combinations of different regions of genioglossus, not only between the shallow, horizontal and deep, oblique fibres, but also between anterior and posterior regions of the muscle, with the number of regions moving increasing with OSA severity. In the present study, we stimulated genioglossus intramuscularly in each of these four regions and measured the evoked movement of the tongue from an accelerometer placed on the posterosuperior surface of the tongue. The aim of this study was to characterise the effect of regional activation of genioglossus on the movement of the tongue in healthy individuals. In previous studies, the stimulus intensity was set at the maximum that could be comfortably tolerated, or higher at close to arousal threshold during sleep, which likely recruited large proportions of motor units across the whole muscle. Here, we stimulated the genioglossus at motor threshold to localise the recruitment of motor units to each of the four regions.
Section snippets
Materials and methods
Ten healthy adults without any history of neuromuscular or sleep disorders were recruited (see Table 1). All procedures were approved by the University of New South Wales Human Research Ethics Committee (HC11280) and conducted in accordance with the Declaration of Helsinki (2008). Participants gave informed consent in writing.
Participant characteristics
The study participants were non-obese men and women aged between 26 and 59 years (Table 1). The stimulation protocol was well tolerated by most participants. However, for participant seven, insertion of the needle electrode into the anterior and posterior regions of genioglossus resulted in painful sensations in the tongue and jaw. This pain persisted despite no electrical stimulation of the muscle. Therefore, the needle electrode was removed and the participant did not continue with the
Discussion
In this study, we measured acceleration of the surface of the tongue as the genioglossus was electrically stimulated at motor threshold in both anterior and posterior regions of the muscle. The lowest current amplitude required to evoke a visible movement in the ultrasound scans was ∼80% higher for anterior than posterior sites. Stimulated contractions generally evoked an anterior acceleration of the posterosuperior surface of the tongue in the stimulus-triggered average responses. All
Author contributions
L.E.B., S.C.G., and J.E.B. performed conceptualization. L.D.W. and P.P.H. developed resources and performed validation. L.D.W., P.P.H., D.J.E., L.E.B., S.C.G. and J.E.B. performed methodology and investigation. B.L.L. performed formal analysis, writing - original draft, and visualization. B.L.L., L.D.W., P.P.H., D.J.E., L.E.B., S.C.G. and J.E.B performed writing - reviewing and editing.
Declarations of Competing Interest
D.J.E. has a Cooperative Research Centre (CRC)-P grant, a joint Australian Government, Academia and Industry collaboration (Industry partner Oventus Medical), receives research income from Bayer and Apnimed, and serves as a consultant outside the submitted work. L.D.W. works as a consultant outside the scope of the submitted work.
Acknowledgements
This work was funded by the National Health and Medical Research Council (NHMRC) of Australia. D.J.E. is supported by a NHMRC Senior Research Fellowship (1116942) and an Investigator Grant (1196261). L.E.B. is supported by a NHMRC Senior Research Fellowship (1077934) and an Investigator Grant (1172988).
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