Sleep/Wake Firing Patterns of Human Genioglossus Motor Units

Abstract

Although studies of the principal tongue protrudor muscle genioglossus (GG) suggest that whole muscle GG electromyographic (EMG) activities are preserved in nonrapid eye movement (NREM) sleep, it is unclear what influence sleep exerts on individual GG motor unit (MU) activities. We characterized the firing patterns of human GG MUs in wakefulness and NREM sleep with the aim of determining 1) whether the range of MU discharge patterns evident in wakefulness is preserved in sleep and 2) what effect the removal of the "wakefulness" input has on the magnitude of the respiratory modulation of MU activities. Microelectrodes inserted into the extrinsic tongue protrudor muscle, the genioglossus, were used to follow the discharge of single MUs. We categorized MU activities on the basis of the temporal relationship between the spike train and the respiration cycle and quantified the magnitude of the respiratory modulation of each MU using the eta ( 2 ) index, in wakefulness and sleep. The majority of MUs exhibited subtle increases or decreases in respiratory modulation but were otherwise unaffected by NREM sleep. In contrast, 30% of MUs exhibited marked sleep-associated changes in discharge frequency and respiratory modulation. We suggest that GG MUs should not be considered exclusively tonic or phasic; rather, the discharge pattern appears to be a flexible feature of GG activities in healthy young adults. Whether such flexibility is important in the response to changes in the chemical and/or mechanical environment and whether it is preserved as a function of aging or in individuals with obstructive sleep apnea are critical questions for future research.

A comprehensive assessment of genioglossus electromyographic activity in healthy adults

“…Average multiunit EMG activity was determined for the phasic (i.e., inspiratory) and tonic (i.e., expiratory) portions of each breath cycle. Because breathing frequencies varied between tasks, EMG measures at each electrode location were based on average EMG amplitude for 10 consecutive breaths (Mateika et al 1999;Eastwood et al 2003;Saboisky et al 2006Saboisky et al 2007Bailey et al 2007;Richardson and Bailey 2010). Because subtle differences in electrode impedance may alter the signal in terms of raw voltage, EMG values were normalized with regard to the regional maximal EMG activity (%maximum) and averaged across breaths.…”

“…In view of the muscle's role as an airway dilator, the preponderance of research has focused on electromyographic (EMG) activity during sleep and wakefulness when subjects are in the supine or side-lying position (Eastwood et al 2003;Malhotra et al 2004;Fogel et al 2005;Bailey et al 2007;Eckert et al 2009;Wilkinson et al 2010;Jordan et al 2010;Richardson and Bailey 2010;Saboisky et al 2010;Laine and Bailey 2011;Trinder et al 2013). Numerous other studies have incorporated manipulations that impact upon respiratory-related GG activity, including head/body position (i.e., head up vs. head back; upright vs. supine) (Douglas et al 1993;Wasicko et al 1993;Ono et al 1996;Otsuka et al 2000;Tsuiki et al 2000;Williams et al 2000;Pae et al 2002Pae et al 2004Takahashi et al 2002;Walsh et al 2008), assessment of EMG activity in multiple muscle regions (Eastwood et al 2003;Wilkinson et al 2008Wilkinson et al 2010Nicholas et al 2010;Richardson and Bailey 2010;McSharry et al 2013;Trinder et al 2013), and in different tasks (i.e., rest breathing, voluntary hyperventilation, maximal inspiratory effort, or exercise) (Mezzanotte et al 1992;Williams et al 2000;Eastwood et al 2003;Walls et al 2013).…”

Dissociation of electromyogram and mechanical response in sleep apnoea during propofol anaesthesia

“…These motor units are coordinated by complex premotor networks [29,44] that may be affected by anaesthesia [45]. The activity of different GG motor units changes differently during the transition from wakefulness to sleep [46][47][48]. Accordingly, the response of the GG to the transitions between sleep and wakefulness includes reorganisation of the pattern of motor unit activation within the muscle.…”

Recruitment and rate-coding strategies of the human genioglossus muscle

“…We hypothesized that the different classes of motor units, previously described (38), would respond as a single population through increases in rate coding (increased firing frequency) and earlier activation of active units, together with recruitment of additional inspiratory phasic units under higher conditions of elevated CO 2 (10). In addition, because premotor inputs and their various thresholds for activation may alter the activation patterns (6,22), we hypothesized a marked reduction in the firing rates and derecruitment of inspiratory units with CPAP. Some of the results of these studies have been previously reported in the form of abstracts (37,42).…”