Journal of Applied Physiology
Vol. 82, No. 2, pp. 584-591, February 1997
CONTROL OF BREATHING, CIRCULATION, AND TEMPERATURE

Respiratory function of velopharyngeal constrictor muscles during wakefulness in normal adults

Sandrine H. Launois^1,3, Judy Tsui^1,3, and J. Woodrow Weiss^1,2,3

¹ Charles A. Dana Research Institute and Harvard-Thorndike Laboratory of Beth Israel Hospital, ² Beth Israel Hospital Sleep Disorders Center, and ³ Department of Medicine, Beth Israel Hospital, Harvard Medical School, Boston, Massachusetts 02215

ABSTRACT

INTRODUCTION

METHODS

RESULTS

DISCUSSION

ACKNOWLEDGEMENTS

FOOTNOTES

REFERENCES

ABSTRACT

Launois, Sandrine H., Judy Tsui, and J. Woodrow Weiss. Respiratory function of velopharyngeal constrictor muscles during wakefulness in normal adults. J. Appl. Physiol. 82(2): 584-591, 1997.The levator veli palatini (LVP) and the superior pharyngeal constrictor (SPC) influence velopharyngeal patency and soft palate position, but their behavior during respiration is incompletely characterized. To further clarify their respiratory function, we recorded electromyographic activity (EMG) in the LVP and the SPC in awake normal subjects breathing orally. EMG data were obtained in six subjects for the LVP and in nine subjects for the SPC. EMG activity and timing and ventilation were measured during isocapnic hypoxia and hyperoxic hypercapnia. Phasic EMG activity was inconsistently present during unstimulated oral breathing. Timing of EMG phasic activity was variable for both muscles. Peak LVP activity was mainly or exclusively expiratory in three of six subjects. Peak SPC activity was mainly or exclusively expiratory in five of nine subjects. With chemostimulation, recruitment of phasic activity was observed in the LVP in four of six subjects and in the SPC in five of nine subjects. Tonic activity increased in four of six subjects for the LVP and in three of nine subjects for the SPC. However, the response was alinear, and intersubject as well as breath-to-breath variability was substantial. In conclusion, LVP and SPC are characterized by the high inter- and intrasubject variability of EMG activity, timing of activation, and response to chemostimulation.

upper airway; soft palate; levator veli palatini; superior pharyngeal constrictor; respiration; chemostimulation; electromyography

INTRODUCTION

THE IMPORTANCE of the velopharyngeal region in the pathophysiology of sleep-disordered breathing has been amply demonstrated. In awake normal subjects as well as sleep apnea patients, the retropalatal region is the narrowest pharyngeal segment during nasal breathing (24). Although collapse can occur in the oropharynx or in the hypopharynx, the velopharynx is frequently a primary site of obstruction during sleep in apneic patients, and transpalatal resistance increases with sleep onset in >50% of normal men (10, 19). In addition, narrowing at the velopharyngeal level may precipitate oro- or hypopharyngeal collapse. Velopharyngeal mechanics are controlled by nonneuromuscular factors such as lung volume and by the activity of the velopharyngeal musculature. The contribution of constrictor muscles to the pathophysiology of sleep-induced changes in upper airway dynamics has received little attention. These muscles play a fundamental role in nonrespiratory functions of the upper airway. Soft palate position is regulated by complex interactions between velopharyngeal constrictor muscles, the levator veli palatini (LVP) and the superior pharyngeal constrictor (SPC), and velopharyngeal dilator muscles, the palatopharyngeus and palatoglossus (7, 13). The respiratory function of the LVP and SPC has not been investigated in detail, but respiratory-related activity has been recorded in both muscles. The SPC exhibits phasic expiratory activity during wakefulness in normal adults during forceful breathing, although no data are available during tidal breathing (23). The LVP respiratory-related activity appears to be more variable: some authors failed to record any phasic activity (8, 12), whereas others demonstrated that phasic activity can be inspiratory, expiratory, or variable and is strongly dependent on the route of breathing (6, 18, 20, 27). Regardless of the phase pattern, tonic and phasic electromyographic (EMG) activity in both muscles are likely to affect velopharyngeal dimensions substantially. To clarify LVP and SPC respiratory function, we recorded their EMG activity in 10 normal adults during wakefulness and assessed their response to hypoxia and hypercapnia.

METHODS

Subjects

Table 1. Subject characteristics Subject No. Sex Age, yr BMI, kg/m2  E/PETCO2, l · min1 · Torr1  E/SaO2, l · min1 · %1 1 M 24 23.8 0.93  0.14 2 F 22 20.4 1.50  0.25 3 M 31 22.3 0.95  0.39 4 F 31 23.2 2.77  0.13 5 F 38 22.1 2.96  1.21 6 M 33 20.3 1.47  1.30 7 F 19 18.9 1.19  0.84 8 M 31 26.6 1.22  1.12 9 F 26 22.1 1.06  0.17 10 M 28 22.4 2.71  0.81 Mean ± SD 28.3 ± 5.7  22.2 ± 2.1  1.68 ± 0.81   0.64 ± 0.47 M, male; F, female; BMI, body mass index; E, minute ventilation; PETCO2, end-tidal PCO2; SaO2, arterial O2 saturation.

Measurements

Experimental Protocol

Data Analysis

EMG signals were obtained in 6 of 10 subjects for the LVP and in 9 of 10 subjects for the SPC. In subject 1, one wire was dislodged during the first hypoxic challenge, and SPC EMG signal during hypoxia could not be analyzed.

The integrated signal was used to quantify EMG activity. Electrical and system baselines did not change throughout the study, and thus electrical zero was used as the reference for measurements. EMG activity was expressed as a percentage of the maximum respiratory-related activity observed during the four trials. Most subjects displayed maximum respiratory activity during hypercapnia for both muscles. Tonic activity was defined as the minimum EMG value and phasic activity as the difference between the maximum EMG value and the tonic activity.

Breaths with unequivocal monophasic activity were selected for phase-pattern analysis. For each subject, 10-46 breaths were selected and grouped on the basis of the levels of chemostimulation: normoxic normocapnia (Sa_O2 >95%, PET_CO2 45 Torr); normoxic mild hypercapnia (Sa_O2 >95%, PET_CO2 56 Torr); normoxic moderate hypercapnia (Sa_O2 >95%, PET_CO2 >56 Torr); normocapnic mild hypoxia (Sa_O2 95%, PET_CO2 45 Torr); and normocapnic moderate hypoxia (Sa_O2 89%, PET_CO2 45 Torr). For each sample, the number of breaths with monophasic EMG activity varied from 0 to 21. The relationship between EMG activity and the respiratory cycle was analyzed for each of these five groups. Timing of peak EMG activity was determined for the selected breaths. Peak activity was considered predominantly expiratory or predominantly inspiratory if it was measured during expiration or inspiration, respectively, in >50% of the selected breaths.

The relationship between EMG activity and PET_CO2 and between EMG activity and Sa_O2 was tested by using the least squares method. For statistical analysis as well as graphic representation (see Figs. 2, 3, 4, 5), phasic and tonic activity for each breath, regardless of its inspiratory or expiratory nature, were considered and data from the two trials were combined. A P value of 0.05 or less was considered significant. Data are presented as means ± SD.

RESULTS

Ventilatory Response to Chemical Stimulation

1

1

1

1

EMG Activity During Quiet Breathing

Timing of EMG Phasic Activity

Table 2. Phase pattern of EMG peak activity: effect of chemostimulation Subject No. Percentage of Breaths With Expiratory Peak Activity A B C D E Levator veli palatini 1 NA 20 6 0 0 2 100 89 86 100 86 3 43 93 100 75 30 5 57 26 NA 56 43 8 NA NA 20 NA NA 10 NA 71 100 NA 38 Superior pharyngeal constrictor 1 NA 50 0 NA NA 2 20 33 20 50 100 4 100 33 0 100 NA 5 0 18 NA 56 NA 6 NA 88 75 100 67 7 20 NA NA 100 100 8 NA 0 14 0 17 9 33 100 0 29 56 10 NA 100 89 NA 100 A, normal PETCO2, normal SaO2; B, mild hypercapnia, normal SaO2; C, moderate hypercapnia, normal SaO2; D, normal PETCO2, mild hypoxia; E, normal PETCO2, moderate hypoxia; NA, no phasic or bi- phasic EMG activity.

Table 3. Phase pattern of EMG peak activity: overall trend Subject No. Percentage of Breaths With Expiratory Peak Activity SPC LVP 1 0 5.6 2 81.8 50.0 3 NA 100 4 22.2 NA 5 38.7 45.2 6 65.2 NA 7 86.2 NA 8 4.0 0 9 87.5 NA 10 100 77.2 Mean ± SD 54.0 ± 38.5  46.4 ± 39.1 SPC, superior pharyngeal constrictor; LVP, levator veli palatini.

In all subjects, and for both muscles, a biphasic discharge pattern was observed occasionally for a single breath. In subject 8, a consistent biphasic pattern was noted in the LVP during hypoxia but not during hypercapnia. In subject 3, LVP was phasically active during expiration and inspiration during the first hypoxic challenge. With progressive hypoxia, inspiratory activity increased, whereas expiratory bursts of EMG activity disappeared (Fig. 1).

LVP Response to Chemical Stimulation

SPC Response to Chemical Stimulation

DISCUSSION

In these normal awake subjects, we found that, while seldom present during quiet oral breathing, phasic activation of the LVP and SPC appeared during progressive isocapnic hypoxia and hyperoxic hypercapnia. However, in our subjects, respiratory activity in these muscles was characterized by marked inter- and intrasubject variability. EMG responses to chemostimulation were brisk and linear in some individuals and weak or alinear in others. In some subjects, phasic and tonic activity disappeared despite progressive hypoxia and hypercapnia. Some subjects responded to one stimulus but not to the other. Variability was also observed in the phase pattern: most subjects displayed activity during both inspiration and expiration.

Although nonneuromuscular factors influence pharyngeal cross-sectional area, palatal dilator muscle activity is considered to be the main determinant of velopharyngeal patency throughout the respiratory cycle (16). Those dilator muscles are thought to counteract intraluminal subatmospheric pressure by producing phasic inspiratory activity, although the role of tonic activity has recently been stressed (26). Constrictor velopharyngeal muscles have received little attention. However, there is evidence to suggest that their participation in velopharyngeal mechanics should be carefully examined. Velopharyngeal constrictor muscles consist of the LVP and the SPC. Activation of the LVP moves the soft palate rostrally and posteriorly, allowing velopharyngeal closure during swallowing and phonation (7). SPC contraction narrows the velopharynx, and its palatal insertion pulls the soft palate posteriorly (7). Phasic activity has been demonstrated in the SPC during quiet breathing during wakefulness in a previous study (9). LVP respiratory-related activity has also been recorded in normal subjects during quiet breathing (3, 18, 28). Our results confirm the presence of respiratory activity in both muscles. In most previous studies, LVP and SPC respiratory activity appeared to be expiratory (3, 8, 23). However, recent preliminary reports suggest that timing of phasic activity is more variable than previously reported (25, 27). In the present study, phasic activity in both muscles was inspiratory, expiratory, biphasic, or variable. LVP and SPC activation are likely to affect velopharyngeal geometry or mechanics at any point during the respiratory cycle. As the main palatal muscle, LVP regulates route of breathing by modifying soft palate position (3, 7, 27). During oral breathing, inspiratory contraction of the LVP could represent active facilitation of oral airflow. Alternatively, the LVP could be activated during inspiration in response to caudal tug of the soft palate. With increasing respiratory efforts during chemical stimulation, EMG activity would increase to counteract passive stretching. If biomechanical action of the SPC is considered alone, the benefit of inspiratory contraction is not apparent. Data obtained with various preparations suggest, however, that the net mechanical effect of a muscle contraction strongly depends on the activity of other upper airway muscles (1, 5). Synergistic action of the SPC with the LVP, palatoglossus, or palatopharyngeus could, therefore, also tend to decrease resistance to oral airflow. In addition to inspiratory activity, our subjects also demonstrated expiratory activation of the LVP and SPC. Expiratory airflow is, in part, regulated by laryngeal and hypopharyngeal resistance, determined by the combination of abductor muscle relaxation and adductor muscle contraction (5, 15). Further modulation of expiratory flow could be achieved by activation of pharyngeal constrictors. Last, activation of constrictor muscles during expiration may affect velopharyngeal air space by altering the length of dilator muscles and modifying their mechanical action. Contraction of these muscles during expiration decreases the velopharyngeal area, thus affecting inspiratory dynamics. Indeed, it has recently been demonstrated that during wakefulness, minimal airway size is seen at the end of expiration in normal subjects and sleep apnea patients (24). Even in the absence of phasic activation, these muscles could affect the size of the upper airway by the level of their tonic activity. However, in the absence of a biomechanical model of upper airway muscles, the effect of constrictor muscle activation on inspiratory mechanics cannot be predicted.

The variability exhibited by LVP and SPC respiratory activity (variable levels of activation during quiet breathing, amplitude and direction of the response to chemostimulation, timing with respect to the respiratory cycle) raises concerns about the validity of our recordings. We believe, however, that technical difficulties are not likely to account for this variability. Electrodes were inserted following a standard method (8, 9), and preparatory cadaver dissections confirmed that our technique was adequate. Furthermore, the presence of EMG activity during voluntary activation ensured that the wire electrodes were in place. Correct placement of the electrodes was also verified visually at the end of the study, although speech maneuvers were not repeated. We cannot, therefore, exclude the possibility that a wire may have been partially dislodged in some patients. Electrical activity from contiguous muscles is unlikely to explain our findings. At the retropalatal level, the SPC is the sole muscle of the posterior pharyngeal wall. To record from the LVP, electrodes are inserted in the levator dimples. In this area of the velum, fibers from the TVP are tendinous and other palatal muscles insert more laterally (palatoglossus, palatopharyngeus) or more posteriorally (musculus uvulae) than the LVP. We are, therefore, confident that electrodes were properly inserted and that the variability of our data reflects variability in LVP and SPC activity from subject to subject.

Although it has not been reported for the alae nasi, the tensor palatini, or the genioglossus, inter- and intrasubject variability in EMG activity have been observed in an animal preparation for the geniohyoid (30) and in normal human subjects for the thyroarytenoid (15), the arytenoid (14), and, to a lesser degree, for the cricothyroid (31). Like these muscles, the SPC and the LVP, as highly specialized muscles active in numerous nonrespiratory functions, are under strong behavioral control. It is, however, unexpected to find such a degree of intrasubject variability during chemostimulation, when low behavioral influences would be anticipated. In the medulla, pharyngeal motoneurons are located in an area overlapping respiratory centers (4), and respiratory influences on the pharyngeal motoneurons are suggested by respiratory-related electrical activity recorded in pharyngeal muscles. However, suprapontine influences are likely to be predominant in the regulation of these motoneurons, which are involved in voluntary activities such as speech production or swallowing. Discomfort due to the mouthpiece, the nose clips, or hyperventilation may have resulted in behavioral control overriding automatic control of palatal musculature, allowing some subjects to modify the position of their palate. Indeed, during a different experimental protocol, we have observed the effect of discomfort caused by a thin nasopharyngoscope on the LVP EMG activity in subject 10: while he was complaining of discomfort, tonic activity was near maximum value; after adjustment of the scope and relief of discomfort, tonic activity decreased sharply by 75% (unpublished observations). Such abrupt changes in tonic activity were observed during this study in subjects 3 and 5. Furthermore, in subject 3, when the level of tonic activity decreased, phasic activity was "unmasked" (Fig. 6). It is, therefore, possible that phasic response to chemostimulation was obscured by high tonic activity in some subjects. Last, tongue and jaw position were not fixed during the course of the experiment. Given the close interactions between pharyngeal muscles, movements of either of these structure are likely to modify the activity of the SPC and LVP (13). Non-rapid-eye-movement (NREM) sleep provides an opportunity to examine the relative contribution of suprapontine influences and "peripheral" or anatomic factors (jaw or tongue position, for instance) to the variability in muscle activity. There are, however, few data available at the present time. In the only study of SPC activity during sleep, Sauerland et al. (23) observed the persistence of SPC phasic activity in NREM but also noted that this activity could be intermittent in some (but not all) subjects. Tangel et al. (29) reported a consistent decrease in peak LVP activity during NREM sleep, although the amplitude of the decrease was somewhat variable. The issue of possible EMG variability was not addressed in either study, and an experimental protocol aimed at investigating how vigilance affects EMG variability may yield important information.

Variable phase pattern was observed in our subjects for the SPC and the LVP. Similar findings have been reported in animal models and normal adults. In dogs, pharyngeal constrictors are active during expiration but can exhibit inspiratory activity as well (11). In decerebrate artificially ventilated cats, glossopharyngeal motoneurons display inspiratory discharge only, whereas both inspiratory and expiratory bursts are present in the pharyngeal branches of the vagus (4). In normal subjects, during progressive hypercapnia, posterior cricoarytenoid inspiratory activity can be prolonged and persists after the beginning of expiration (2). Previous studies did not show any variability in the relationship of LVP or SPC activity to the respiratory cycle (3, 9, 18, 23, 28). Differences in species, body position, route of breathing, or chemical drive could account for the discrepancy among studies. The significance of shifts in phase pattern of pharyngeal muscles remains unclear.

In conclusion, velopharyngeal constrictors display respiratory activity and respond to chemostimulation. Their electrical activity is remarkably variable, and we suggest that this variability results from strong behavioral influences on pharyngeal motoneurons supplying these muscles. Additional studies of velopharyngeal muscle activity during wakefulness and sleep may provide further evidence of the role of these suprapontine influences.

At this stage, we can only speculate on how the variability that we observed in EMG activity may affect velopharyngeal function. This variability in velopharyngeal musculature activity is likely to contribute to the absence of a consistent relationship between palatal muscle activity and velopharyngeal patency that our laboratory has reported recently in normal awake adults (17). If one assumes that velopharyngeal muscles determine velopharyngeal patency, variable EMG activation would require multiple interaction patterns between local and regional muscles to maintain velopharyngeal patency while behavioral and anatomical factors fluctuate.

Last, the findings of this study should encourage future investigators to take variable EMG activity into account when investigating palatal muscle contribution to transpalatal resistance and velopharyngeal narrowing during sleep.

ACKNOWLEDGEMENTS

This work was supported by National Heart, Lung, and Blood Institute Grant HL-46951. S. H. Launois is a fellow in the Clinical Investigator Training Program: Beth Israel Hospital-Harvard/MIT Health Sciences and Technology, in collaboration with Pfizer, Inc.

FOOTNOTES

Address for reprint requests: S. H. Launois, Pulmonary Div., Dept. of Medicine, Beth Israel Hospital Boston, 330 Brookline Ave., Boston MA 02115 (E-mail: slaunois{at}bidmc.harvard.edu).

Received 27 February 1996; accepted in final form 10 September 1996.

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