Differential effect of sleep-wake states on lingual and dorsal neck muscle activity in rats

Abstract

Postural tone is reduced during slow-wave sleep (SWS) and absent during rapid eye movement sleep (REMS). In obstructive sleep apnea subjects, upper airway dilating muscles, including those of the tongue, show a similar pattern; this contributes to sleep-related airway obstructions. However, in healthy subjects, state-dependent changes in the activity of pharyngeal muscles are variable. In seven chronically instrumented Sprague–Dawley rats, an animal model used to study sleep and sleep-disordered breathing, we quantified lingual and postural muscle activity across the sleep-wake states by measuring the root mean square levels of the electromyograms (EMG) in successive 10 s intervals collected during 2 h of recording at a constant circadian time (1–3 p.m.). The nuchal EMG was low and steady during SWS and further reduced with occasional twitches during REMS. In contrast, the mean lingual EMG during SWS was only 5.9 ± 1.6% (S.E.) of its mean in wakefulness, and during REMS, it increased to 46 ± 15% (S.E.) (p < 0.03) due to the appearance of phasic bursts, the intensity of which progressively increased. The lingual and nuchal activities also had different time courses during state transitions. In obstructive sleep apnea subjects, the sleep-wake changes in the activity of pharyngeal muscles may become similar to those in postural muscles as a result of pharyngeal tone adaptations to the disorder.

Introduction

During wakefulness (W), orofacial muscles innervated by the trigeminal, facial, vagal and hypoglossal nerves subserve multiple functions, such as deglutition, swallowing and phonation, each of them requiring coordination with breathing (Travers and Jackson, 1992, Feroah et al., 2002; see also Gestreau et al. and Yamada et al. in this special issue). In sleep, these functions are suppressed, or cease altogether (e.g., Anderson et al., 1995), whereas breathing continues, becoming the main function of many orofacial muscles. In healthy subjects, the impact of the activity, or lack thereof, in upper airway muscles on breathing during sleep is minor. However, in subjects with a narrow and/or collapsible airway, adequate level of activity in upper airway muscles, especially those in the pharyngeal region, is critical for the maintenance of upper airway patency. Indeed, in subjects with the obstructive sleep apnea syndrome (OSAS), sleep-related airway obstructions and flow limitations coincide with decrements of pharyngeal muscle tone (e.g., Anch et al., 1981, Hendricks et al., 1987, Wiegand et al., 1990a, Okabe et al., 1994), and termination of obstructive episodes is associated with activation of pharyngeal muscles (Remmers et al., 1978). Moreover, stimulation of upper airway muscles improves airway patency and can prevent upper airway collapse (Schwartz et al., 1993, Schwartz et al., 1996).

OSAS subjects have increased pharyngeal muscle activity during W (Suratt et al., 1988, Sériès et al., 1989, Mezzanotte et al., 1992, Hendricks et al., 1993). This activity then gradually decreases during transition into slow-wave sleep (SWS) and rapid eye movement sleep (REMS) (Hendricks et al., 1993, Okabe et al., 1994, Mezzanotte et al., 1996, Katz and White, 2003; reviewed by Kubin and Davies, 2002). This pattern is similar to that of postural muscles that have high tonic and phasic activities during W, reduced and steady activity during SWS, and minimal activity (atonia) with occasional twitches during REMS (e.g., Gardner and Grossman, 1975). In contrast, in healthy subjects, the activity of the muscles of the tongue, whose stiffness and position significantly contribute to the maintenance of airway patency (Brouillette and Thach, 1979, Fregosi and Fuller, 1997, Schwartz et al., 1998), is reported to increase, decrease or not change across the sleep-wake states. For example, in humans, the activities of the genioglossus and geniohyoid, two major muscles innervated by cranial nerve XII, may increase (Basner et al., 1991, Tangel et al., 1992, Shea et al., 1999), decrease (Worsnop et al., 1998, Malhotra et al., 2000) or change little (Katz and White, 2003) during SWS. Then, in REMS, the activity is also reported to increase (Wiegand et al., 1990b), decrease (Wiegand et al., 1991) or not change (Shea et al., 1999), with the variability of the results caused, at least in part, by the varying intensity of phasic events during different REMS periods. In other mammals with a normal upper airway, genioglossal and other pharyngeal muscle activities decrease during SWS and then may increase (Richard and Harper, 1991, Hendricks et al., 1993) or decrease (Plowman et al., 1990, Feroah et al., 2001) during REMS. In the rat, a commonly used animal model for studies of the central regulation of both sleep and breathing, systematic observations of lingual muscle activity across the sleep-wake states are limited, but both increases (Megirian et al., 1978) and decreases (Megirian et al., 1985, Morrison et al., 2003) during REMS have been reported. Thus, the pattern of lingual muscle activity across the sleep-wake states in subjects with a normal airway is not clear.

Our goal was to quantify the levels of activity in lingual muscles across the sleep-wake states in normal, adult rats under undisturbed experimental conditions, and compare them to state-dependent changes in the activity of dorsal neck muscles, which are commonly measured as an index of postural tone. A preliminary report has been published (Lu et al., 2004).