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(O2), 160 +/- 12 mm Hg) and in mild isocapnic hypoxia (Pa(O2), 69 +/- 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.

Figure 1.

Representative integrated (i) and raw EMG recordings of extrinsic and intrinsic tongue muscles, esophageal pressures (Pes), and arterial blood pressure (BP) in a vagi-intact animal obtained under control gas conditions (30% O₂, 0% CO₂, balance N₂) and mild hypoxia (16% O₂, 3% CO₂, balance N₂).

Figure 2.

Representative integrated EMG recordings of extrinsic and intrinsic tongue muscles and Pes in a vagi-intact animal in the control gas condition and mild hypoxia, comparing burst envelopes with (black traces) and without (gray traces) airway occlusion.

Figure 3.

Mean (and SD) minute Pes (cm H₂O/minute) and extrinsic and intrinsic EMG activities (% of max) with (black squares) and without (gray circles) airway occlusion as a function of Pa_O2. ⁺Indicates a significant difference (p < 0.01) for a given variable relative to the control gas condition. ^γIndicates a significant difference (p < 0.016) between occlusion and no-occlusion conditions for a given variable.

Figure 4.

Mean (and SD) onset time (seconds) of extrinsic (light gray) and intrinsic (dark gray) tongue muscle activities under control gas conditions and in mild hypoxia in vagi-intact preparations. ^ξIndicates a significant difference (p < 0.01) in the onset of extrinsic tongue muscle activities relative to the onset of inspiration (denoted by the negative phase of the Pes swing).

Figure 5.

Mean (and SD) rate of rise (% of max) of Pes (white), extrinsic (light gray), and intrinsic (dark gray) tongue muscle activities in the control gas condition and mild hypoxia in vagi-intact preparations. ⁺Indicates a significant difference (p < 0.01) in rate of rise of extrinsic versus intrinsic tongue muscle activities under a given condition. ^γIndicates a significant difference in the rate of rise of Pes with respect to the control gas condition.

Figure 6.

Mean (and SD) onset time of extrinsic (light gray) and intrinsic (dark gray) tongue muscle activities in the control condition and mild hypoxia postvagotomy. ⁺Indicates a significant difference (p < 0.01) in onset time of extrinsic versus intrinsic tongue muscle activities in a given condition. ^γIndicates a significant difference for a given variable with respect to the control gas condition.

Figure 7.

Mean (and SD) of rate of rise (% of max) of Pes (white) and extrinsic (light gray) and intrinsic (dark gray) tongue muscle activities in the control gas condition and mild hypoxia postvagotomy. ^γIndicates a significant difference for a given variable with respect to the control gas condition.