Recruitment and rate-coding strategies of the human genioglossus muscle

Abstract

Saboisky JP, Jordan AS, Eckert DJ, White DP, Trinder JA, Nicholas CL, Gautam S, Malhotra A. Recruitment and rate-coding strategies of the human genioglossus muscle. J Appl Physiol 109: 1939-1949. First published October 14, 2010 doi:10.1152/japplphysiol.00812.2010.-Single motor unit (SMU) analysis provides a means to examine the motor control of a muscle. SMUs in the genioglossus show considerable complexity, with several different firing patterns. Two of the primary stimuli that contribute to genioglossal activation are carbon dioxide (CO 2) and negative pressure, which act through chemoreceptor and mechanoreceptor activation, respectively. We sought to determine how these stimuli affect the behavior of genioglossus SMUs. We quantified genioglossus SMU discharge activity during periods of quiet breathing, elevated CO2 (facilitation), and continuous positive airway pressure (CPAP) administration (inhibition). CPAP was applied in 2-cmH2O increments until 10 cmH2O during hypercapnia. Five hundred ninety-one periods (each ϳ3 breaths) of genioglossus SMU data were recorded using wire electrodes(n ϭ 96 units) from 15 awake, supine subjects. Overall hypercapnic stimulation increased the discharge rate of genioglossus units (20.9 Ϯ 1.0 vs. 22.7 Ϯ 0.9 Hz). Inspiratory units were activated ϳ13% earlier in the inspiratory cycle, and the units fired for a longer duration (80.6 Ϯ 5.1 vs. 105.3 Ϯ 4.2% inspiratory time; P Ͻ 0.05). Compared with baseline, an additional 32% of distinguishable SMUs within the selective electrode recording area were recruited with hypercapnia. CPAP led to progressive SMU inhibition; at ϳ6 cmH 2O, there were similar numbers of SMUs active compared with baseline, with peak frequencies of inspiratory units close to baseline, despite elevated CO 2 levels. At 10 cmH2O, the number of units was 36% less than baseline. Genioglossus inspiratory phasic SMUs respond to hypercapnic stimulation with changes in recruitment and rate coding. The SMUs respond to CPAP with derecruitment as a homogeneous population, and inspiratory phasic units show slower discharge rates. Understanding upper airway muscle recruitment/derecruitment may yield therapeutic targets for maintenance of pharyngeal patency.

Effects of tongue position and lung volume on voluntary maximal tongue protrusion force in humans

“…Second, volitional control of the human tongue may be altered by inputs from pulmonary and chest wall receptors (Saito et al, 2002). Respiratory rhythm (Saboisky et al, 2006(Saboisky et al, , 2010Sauerland and Mitchell, 1975;Tsuiki et al, 2000) is modulated by feedback from pulmonary stretch receptors (e.g. Cohen, 1969;Colridge and Colridge, 1986;Hwang and St John, 1987;Saito et al, 2002) and this has a greater inhibitory effect on the discharge of hypoglossal motoneurons compared to phrenic motoneurons (Hwang and St John, 1987;Kuna, 1986;Sica et al, 1984;van Lunteren et al, 1984).…”

Phonation-related rate coding and recruitment in the genioglossus muscle

“…Because minimum firing rate is inversely related to the duration of the AHP after the action potential, GG motoneurons may possess briefer period AHPs than FDI motoneurons. Remarkably, although firing rate modulation is evident here in the context of phonation and in protrusion (Bailey et al 2007b), there is little evidence of rate modulation in respiration-related contexts (Nicholas et al 2010; Richardson and Bailey 2010; Saboisky et al 2010). This disparity in GG motor unit firing rates for volitional versus respiratory conditions suggests that firing rates in the GG are more likely a function of the source/s of drive impinging on the pool than whether the pool has a cranial/ spinal location.…”

Neural Control of the Upper Airway: Respiratory and State‐Dependent Mechanisms

“…Despite extensive body of research, the impact on the size and stiffness of the upper airway of many lesser muscles has not been studied (Table 1). Nevertheless, it is of note that muscle fibers of the tongue can be functionally classified as causing a tongue-protrusive or tongue-retractive action, and these functional types have been related to predominantly inspiratory or predominantly expiratory patterns of activity (e.g., 109, 333, 453, 556, 597). However, data indicate that protrusor and retractor muscles are simultaneously, rather than reciprocally, activated when they act to protect the airway from collapse, and such an action both stiffens the airway walls and enlarges the airway lumen (159).…”