PO₂-dependent Changes in Intrinsic and Extrinsic Tongue Muscle Activities in the Rat

Abstract

Rationale: Historically, respiratory-related research in sleep apnea has focused exclusively on the extrinsic tongue muscles (i.e., genioglossus, hyoglossus, and styloglossus). Until recently, the respiratory control and function of intrinsic tongue muscles (i.e., inferior and superior longitudinalis, transverses, and verticalis), which comprise the bulk of the tongue, were unknown. Objectives: The current study sought to determine if extrinsic and intrinsic tongue muscles are coactivated in conditions of hypoxemia comparable to that experienced by adults with obstructive sleep apnea. Measurements: Esophageal pressure and EMG activity of an extrinsic (hyoglossus) and an intrinsic (superior longitudinal) tongue muscle were studied in anesthetized, tracheotomized, spontaneously breathing rats. Average EMG activity was compared in a control gas condition (Pa O 2 , 160 Ϯ 12 mm Hg) and in mild isocapnic hypoxia (Pa O 2 , 69 Ϯ 7.2 mm Hg), with and without brief (3-breath) airway occlusions, pre-and postbilateral vagotomy. Main Results: (1 ) intrinsic and extrinsic tongue muscles are coactivated in mild hypoxia, (2 ) airway occlusion increased the activities of intrinsic retractor muscles in mild hypoxia, and (3 ) extrinsic retractor muscles have a steeper rate of rise of activity and an earlier burst onset relative to intrinsic retractor activities in mild hypoxia. Conclusions: These findings support our working hypothesis that airway patency is maintained not simply by activation of extrinsic tongue muscles but by the coactivation of intrinsic and extrinsic protrudor and retractor muscles. Keywords: EMG; hypoxia; sleep apneaThe tongue participates in a range of complex oromotor behaviors, including mastication, swallowing, and respiration. Functional deficits in tongue movement contribute to a host of disorders, including obstructive sleep apnea (1), dysarthria, and dysphagia (2-4). To date, studies that have examined the respiratoryrelated control of the tongue have focused primarily on the extrinsic tongue protrudor muscle, the genioglossus. As a result of this work, we know that the genioglossus is phasically active during the respiratory cycle and that its discharge onset precedes the onset of inspiratory airflow, stabilizing the airway for the negative pressure generated by the diaphragm (5-7). Although the genioglossus muscle is an important tongue muscle, it is only one of eight paired muscles that comprise the bulk of the tongue (8). Recent work in mammals has shown that the genioglossus and tongue retractor muscles are coactive in eupnea and hypercapnia (9-12), and that this coactivation improves pharyngeal airway patency (13,14). These findings confirm that numerous tongue muscles are involved in the maintenance of airway pat-(Received in original form November 19, 2004; accepted in final form March 12, 2005) Supported by the National Institutes of Health grants DC-05728 and HL-56876. Evidence of intrinsic tongue muscle activities in hypercapnia indicates that these muscles also have the potential to con...

Respiration-related discharge of hyoglossus muscle motor units in the rat

“…HG muscle and motor unit discharge patterns, and the contributions of rate coding and recruitment to muscle force output. We confirmed earlier work indicating that the rodent HG muscle contracts primarily during the inspiratory phase of the respiratory cycle in rats (Bailey and Fregosi 2004;Bailey et al 2005;Fuller et al 1998;Fuller and Fregosi 2000; and in human subjects studied during hypercapnia (Mateika et al 1999). This is consistent with our findings here, showing that all 38 motor units discharged during the inspiratory phase of the respiratory cycle.…”

“…The digastric, mylohyoid, and geniohyoid muscles were removed bilaterally to expose the hypoglossal nerves and the HG muscles, as described in detail previously (Bailey and Fregosi 2004;Bailey et al 2001Bailey et al , 2005Fuller et al 1999;John et al 2005). The hypoglossal nerves bifurcate into medial and lateral branches: the former innervates the tongue protrudor muscles (genioglossus, intrinsic tongue protrudor muscles), and the latter innervates the retractor muscles (HG, styloglossus and intrinsic retractor muscles).…”

“…Whole muscle EMG of the HG was recorded in nine of the animals using two fine hook wire electrodes inserted into the muscle belly and spaced about 2 mm apart, as described previously (Bailey and Fregosi 2004;Bailey et al 2005;Fuller et al 1998;Fuller and Fregosi 2000;. The signal was amplified and filtered (30 -300 Hz) and sent in parallel to an oscilloscope and an analog-to-digital converter, and sampled at 5,000 Hz.…”

Influence of tongue muscle contraction and dynamic airway pressure on velopharyngeal volume in the rat

“…The second methodological issue is that the rat pharynx is more rectilinear than the curved human pharynx, but several observations have validated the functional similarities of the rat and human pharynx, particularly with regard to the neural control (1,2,5,6,10,19,33) and mechanical effects (15, 16, 27, 33, 35-37, 45, 46) of extrinsic tongue muscle contraction. The third issue is that the rat epiglottis reaches the caudal margin of the soft palate, which contrasts with the adult human, in whom the epiglottis and soft palate are separated.…”

“…Results for each measured variable were analyzed with two-way repeated-measures ANOVA, with VP segment (i.e., slices [1][2][3][4][5][6][7][8] and stimulation/no-stimulation the main factors. If the results of ANOVA were significant, differences between stimulation and no-stimulation conditions for each slice were evaluated with Bonferroni post hoc tests (Graph Pad Prism Software, San Diego, CA).…”