Wagging the Tongue and Guarding the Airway
Reflex Control of the Genioglossus

John E. Remmers, M.D.

University of Calgary, Calgary, Alberta, Canada

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To serve its dual functions of alimentation and respiration, the pharynx must be collapsible, and the mechanical demands of human speech require an extremely high compliance of the passive pharynx. The passive human pharynx expands from fully closed to one-half maximum cross-sectional area with a 1-2 cm H₂O increase in luminal pressure (1, 2). This floppy airway is nicely stabilized by contraction of pharyngeal muscles while awake, but the high compliance of the passive pharynx becomes a liability during sleep when reduction of muscle activity commonly leads to high resistance or complete occlusion of the airway. Compensatory reflexes acting on pharyngeal dilators appear to play an important role in preventing pharyngeal narrowing while awake (3). For instance, Anch and coworkers noted that supraglottic resistance (RSG) is higher than normal in patients with obstructive sleep apnea (OSA) while awake (4), and Mezzanotte and coworkers (5) reported that the electromyogram (EMG) of the genioglossus is greater than normal in such patients while awake.

In a series of interventional experiments that challenge the patency of the pharynx, Fogel and coworkers (pp. 2025-2030) (6) addressed the remarkable ability of the pharyngeal muscles to guard the highly collapsible pharyngeal airway while awake. Awake normal subjects and patients with OSA received respiratory loading and unloading without changing overall respiratory drive. One key intervention, negative extrathoracic pressure ventilatory assistance (iron lung), unloaded pump muscles but increased RSG, thereby qualitatively separating global actions on the respiratory system from upper airway perturbations. A lovely experimental design was rewarded with equally beautiful results, revealing prominent control of genioglossal activity by autogenic, mechanoreflexes, that is, reflex loops that seem to originate in upper airway mechanoreceptors and control the activity of pharyngeal muscles. Both genioglossal EMG and RSG were greater in patients than in control subjects under all conditions (quiet breathing, iron lung ventilation, helium-oxygen breathing, and resistive loading). Within each group, the EMG displayed a linear dependence on epiglottal pressure (Pepi). Remarkably, over a 10-fold range of RSG, a single continuous regression describes the EMG/RSG data for both groups, with points for loaded and unloaded breathing corresponding closely (see Figure E1 in the online data supplement to this editorial). Thus, the interventions initiated one or more reflexes controlling genioglossal EMG by altering upper airway pressure and/or resistance.

Although Fogel and coworkers (6) state that within each group, EMG correlates best with epiglottic pressure (statistics not provided), our analysis for both groups combined show that EMG correlates at least as closely with RSG (peak EMG/ RSG:r² = 0.930; phasic EMG/RSG:r² = 0.881; peak EMG/ Pepi:r² = 0.738; phasic EMG/Pepi:r² = 0.848). Fogel and coworkers (6) plausibly speculate that receptors transducing upper airway pressure initiate the reflex. However, a dependence of genioglossal EMG on resistance suggests a contribution by afferent information related to airflow. An integration of pressure and airflow signals would provide better control of the airway since both variables change when the caliber of the pharynx changes.

The afferent information driving presumed autogenic pharyngeal reflexes might contribute to conscious respiratory sensations. In a study that parallels Fogel and coworkers (6), McNicholas and coworkers (7) compared the detection of inspiratory resistive loads in normal subjects and patients with OSA. Although the threshold for load detection was higher in patients with OSA than in normal subjects, a single regression described the dependence of threshold on the hypercapnic ventilatory response for both groups.

The study of Fogel and coworkers is the first clear description of a powerful reflex regulating pharyngeal caliber in humans. The reflex is peculiar to wakefulness, being greatly reduced or lost during sleep or anesthesia (8). This aspect of the reflex may signify a crucial role of the higher nervous system. Why such an essential reflex would be dependent on "higher centers" is puzzling. Perhaps, it reflects the rather recent philogenetic "need" for stabilization of the pharynx, since only with the appearance of the highly compliant, speech-based pharynx in humans did pharyngeal collapse become an important threat. Thus, enhancement of reflex control of the relevant muscles might be a recent event in evolutionary time, allowing little time for evolution of neuronal mechanisms robust enough to operate during sleep.

That a single continuous function describes the dependence of genioglossal EMG on RSG across both normal subjects and patients with apnea suggests that the properties of the putative reflex in patients with apnea are unchanged by repeated pharyngeal occlusion and high pharyngeal resistance. This is a surprising feature as most reflexes undergo plastic alterations with repeat stimulation (9); it confirms the biblical view of the importance and diffidence of the tongue.

The tongue is only a tiny part of the body, but it . . . does great things. Among all the parts of the body, the tongue is a wicked world in itself. Wild animals and birds, reptiles and fish can all be trained by man, but nobody can train the tongue. (James 3:8)

	Footnotes

	References

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