Upper airway muscle activity and upper airway resistance in young adults during sleep

Henke, Kathe G. Upper airway muscle activity and upperairway resistance in young adults during sleep. J. Appl. Physiol. 84(2): 486-491, 1998.To determinethe relationship between upper airway muscle activity and upper airwayresistance in nonsnoring and snoring young adults, 17 subjects werestudied during sleep. Genioglossus and alae nasi electromyogramactivity were recorded. Inspiratory and expiratory supraglotticresistance (Rinsp and Rexp, respectively) were measured at peak flow,and the coefficients of resistance(K_insp andK_exp,respectively) were calculated. Data were recorded during control,with continuous positive airway pressure (CPAP), and on the breathimmediately after termination of CPAP. Rinsp during control averaged 7 ± 1 and 10 ± 2 cmH₂O · l¹ · sand K_inspaveraged 26 ± 5 and 80 ± 27 cmH₂O · l¹ · s²in the nonsnorers and snorers, respectively(P = not significant). Onthe breath immediately after CPAP,K_insp did notincrease over control in snorers (80 ± 27 for control vs. 46 ± 6 cmH₂O · l¹ · s²for the breath after CPAP) or nonsnorers (26 ± 5 vs. 29 ± 6 cmH₂O · l¹ · s²).These findings held true for Rinsp.K_exp did notincrease in either group on the breath immediately after termination ofCPAP. Therefore, 1) increases inupper airway resistance do not occur, despite reductions inelectromyogram activity in young snorers and nonsnorers, and2) increases in Rexp and expiratoryflow limitation are not observed in young snorers.

     

Breathing route dependence of upper airway muscle activity during hyperpnea

Exercise (Ex) and hypercapnia (HC) both lead toincreases in ventilation and upper airway muscle (UAM) activity. Todetermine whether different breathing routes (nasal vs. oral) orstimuli produced differential UAM activation, electromyographic (EMG) activity of the alae nasi (AN) and genioglossus (GG) were measured inseven normal subjects seated on a bicycle ergometer. Subjects performedpaired runs during both progressive Ex and HC while breathing throughthe nose alone (N) or the mouth alone (O). During hyperpnea, AN EMG wasgreater when the subjects were breathing via N [81 ± 6%maximum (HC) and 69 ± 7% maximum (Ex)] than when they werebreathing via O [30 ± 5% maximum (HC) and 27 ± 5%maximum (Ex); both P < 0.01],whereas the GG EMG did not differ between N and O. Both AN and GG EMGwere similar for Ex and HC when the subjects were breathing via thesame route. We conclude that UAM activation was independent of thenature of the stimulus. However, the AN muscle but not the GG muscledemonstrated breathing-route dependence of activity.

     

Effect of sleep-induced increases in upper airway resistance on respiratory muscle activity

To investigate the response of inspiratory and expiratory muscles to naturally occurring inspiratory resistive loads in the absence of conscious control, five male "snorers" were studied during non-rapid-eye-movement (NREM) sleep with and without continuous positive airway pressure (CPAP). Diaphragm (EMGdi) and scalene (EMGsc) electromyographic activity were monitored with surface electrodes and abdominal EMG activity (EMGab) with wire electrodes. Subjects were studied in the following conditions: 1) awake, 2) stage 2 sleep, 3) stage 3/4 sleep, 4) CPAP during stage 3/4 sleep, 5) CPAP plus end-tidal CO2 pressure (PETCO2) isocapnic to stage 2 sleep, and 6) CPAP plus PETCO2 isocapnic to stage 3/4 sleep. Inspired pulmonary resistance (RL) at peak flow rate and PETCO2 increased in all stages of sleep. Activity of EMGdi, EMGsc, and EMGab increased significantly in stage 3/4 sleep. CPAP reduced RL at peak flow, increased tidal volume and expired ventilation, and reduced PETCO2. EMGdi and EMGsc were reduced, and EMGab was silenced. During CPAP, with CO2 added to make PETCO2 isocapnic to stage 3/4 sleep, EMGsc and EMGab increased, but EMGdi was augmented in only one-half of the trials. EMG activity in this condition, however, was only 75% (EMGsc) and 43% (EMGab) of the activity observed during eupneic breathing in stage 3/4 sleep when PETCO2 was equal but RL was much higher. We conclude that during NREM sleep 1) inspiratory and expiratory muscles respond to internal inspiratory resistive loads and the associated dynamic airway narrowing and turbulent flow developed throughout inspiration, 2) some of the augmentation of respiratory muscle activity is also due to the hypercapnia that accompanies loading, and 3) the abdominal muscles are the most sensitive to load and CO2 and the diaphragm is the least sensitive.     

Relation between upper airway volume and hyoid muscle length

Previous studies have suggested that the geniohyoid and sternohyoid muscles act to enlarge the upper airway. If correct, there should be an inverse relation between upper airway volume and the length of hyoid muscles. To test this, known volumes of air were injected into or removed from the isolated sealed upper airway of eight pentobarbital sodium-anesthetized cats, and the resultant changes in geniohyoid and sternohyoid length were measured using sonomicrometry. Increases in upper airway volume shortened the geniohyoid in all cats (P less than 0.001) and shortened the sternohyoid in seven of eight cats (P less than 0.01); mean geniohyoid shortening (as a % of resting length) exceeded that of the sternohyoid. Decreases in upper airway volume lengthened the geniohyoid in all cats (P less than 0.001) but caused variable changes in sternohyoid length. Extension of the neck increased the resting lengths of both the geniohyoid (P less than 0.001) and sternohyoid (P less than 0.002). Neck flexion shortened the resting length of both hyoid muscles (P less than 0.001 for both), with the geniohyoid shortening more (as a % of resting length) than the sternohyoid (P less than 0.005). Progressive flexion of the neck from 180 to 90 degrees caused progressive increases in the ratio of changes in muscle length to changes in upper airway volume during airway inflation but did not affect this relation during airway deflation.(ABSTRACT TRUNCATED AT 250 WORDS)     

Upper airway negative-pressure effects on respiratory activity of upper airway muscles

Influence of upper airway negative-pressure change on the respiratory activity of various upper airway muscles was investigated in 13 anesthetized rabbits. Phasic inspiratory activity increased or appeared during virtually all negative-pressure trials in nasolabial, cricothyroid, and posterior cricoarytenoid muscles. No phasic inspiratory activity was seen in the sternothyroid (ST) and sternohyoid (SH) muscles before negative-pressure applications but appeared during 80% of trials in ST and 62% of trials in SH. During maintained negative pressure, a gradual decline in activity was often observed in the nasolabial and laryngeal muscles, whereas a rapid decline in activity was seen in the cervical strap muscles. Reflex effects of negative pressure was markedly reduced or abolished by sectioning the internal branch of the superior laryngeal nerve bilaterally. Reflex augmentation of upper airway muscle activity reported here may have functional significance in the maintenance of upper airway patency. It could prevent upper airway collapse when negative pressure swings in the upper airway increase or facilitate recovery when large negative pressure swings are produced by obstructed inspiratory efforts.     

Upper airway resistance and geniohyoid muscle activity in normal men during wakefulness and sleep

Sleep-related reduction in geniohyoid muscular support may lead to increased airway resistance in normal subjects. To test this hypothesis, we studied seven normal men throughout a single night of sleep. We recorded inspiratory supraglottic airway resistance, geniohyoid muscle electromyographic (EMGgh) activity, sleep staging, and ventilatory parameters in these subjects during supine nasal breathing. Mean inspiratory upper airway resistance was significantly (P less than 0.01) increased in these subjects during all stages of sleep compared with wakefulness, reaching highest levels during non-rapid-eye-movement (NREM) sleep [awake 2.5 +/- 0.6 (SE) cmH2O.l-1.s, stage 2 NREM sleep 24.1 +/- 11.1, stage 3/4 NREM sleep 30.2 +/- 12.3, rapid-eye-movement (REM) sleep 13.0 +/- 6.7]. Breath-by-breath linear correlation analyses of upper airway resistance and time-averaged EMGgh amplitude demonstrated a significant (P less than 0.05) negative correlation (r = -0.44 to -0.55) between these parameters in five of seven subjects when data from all states (wakefulness and sleep) were combined. However, we found no clear relationship between normalized upper airway resistance and EMGgh activity during individual states (wakefulness, stage 2 NREM sleep, stage 3/4 NREM sleep, and REM sleep) when data from all subjects were combined. The timing of EMGgh onset relative to the onset of inspiratory airflow did not change significantly during wakefulness, NREM sleep, and REM sleep. Inspiratory augmentation of geniohyoid activity generally preceded the start of inspiratory airflow. The time from onset of inspiratory airflow to peak inspiratory EMGgh activity was significantly increased during sleep compared with wakefulness (awake 0.81 +/- 0.04 s, NREM sleep 1.01 +/- 0.04, REM sleep 1.04 +/- 0.05; P less than 0.05). These data indicate that sleep-related changes in geniohyoid muscle activity may influence upper airway resistance in some subjects. However, the relationship between geniohyoid muscle activity and upper airway resistance was complex and varied among subjects, suggesting that other factors must also be considered to explain sleep influences on upper airway patency.     

Effects of tracheal airway occlusion on hyoid muscle length and upper airway volume

Complex relationships exist among electromyograms (EMGs) of the upper airway muscles, respective changes in muscle length, and upper airway volume. To test the effects of preventing lung inflation on these relationships, recordings were made of EMGs and length changes of the geniohyoid (GH) and sternohyoid (SH) muscles as well as of tidal changes in upper airway volume in eight anesthetized cats. During resting breathing, tracheal airway occlusion tended to increase the inspiratory lengthening of GH and SH. In response to progressive hypercapnia, the GH eventually shortened during inspiration in all animals; the extent of muscle shortening was minimally augmented by airway occlusion despite substantial increases in EMGs. SH lengthened during inspiration in six of eight animals under hypercapnic conditions, and in these cats lengthening was greater during airway occlusion even though EMGs increased. Despite the above effects on SH and GH length, upper airway tidal volume was increased significantly by tracheal occlusion under hypercapnic conditions. These data suggest that the thoracic and upper airway muscle reflex effects of preventing lung inflation during inspiration act antagonistically on hyoid muscle length, but, because of the mechanical arrangement of the hyoid muscles relative to the airway and thorax, they act agonistically to augment tidal changes in upper airway volume. The augmentation of upper airway tidal volume may occur in part as a result of the effects of thoracic movements being passively transmitted through the hyoid muscles.     

Effects of continuous positive airway pressure on upper airway and respiratory muscle activity

To study the effects of continuous positive airway pressure (CPAP) on lung volume, and upper airway and respiratory muscle activity, we quantitated the CPAP-induced changes in diaphragmatic and genioglossal electromyograms, esophageal and transdiaphragmatic pressures (Pes and Pdi), and functional residual capacity (FRC) in six normal awake subjects in the supine position. CPAP resulted in increased FRC, increased peak and rate of rise of diaphragmatic activity (EMGdi and EMGdi/TI), decreased peak genioglossal activity (EMGge), decreased inspiratory time and inspiratory duty cycle (P less than 0.001 for all comparisons). Inspiratory changes in Pes and Pdi, as well as Pes/EMGdi and Pdi/EMGdi also decreased (P less than 0.001 for all comparisons), but mean inspiratory airflow for a given Pes increased (P less than 0.001) on CPAP. The increase in mean inspiratory airflow for a given Pes despite the decrease in upper airway muscle activity suggests that CPAP mechanically splints the upper airway. The changes in EMGge and EMGdi after CPAP application most likely reflect the effects of CPAP and the associated changes in respiratory system mechanics on the afferent input from receptors distributed throughout the intact respiratory system.     

Upper airway muscle activity during nasal occlusion in newborn babies

Submental electromyorgams (SM EMG) were recorded from 20 preterm babies (gestational age 30 +/- 2 wk, postmenstrual age at study 35 +/- 2 wk) (mean +/- SD) and 3 full-term infants (7-14 days old). SM EMG was evaluated during eupnea and brief experimental airway occlusion. Phasic inspiratory SM EMG was rarely seen during eupnea. SM EMG tended to increase on the first occluded effort, although this increase was not statistically significant in most babies. All infants showed progressive breath-by-breath augmentation of phasic SM EMG during occlusions in rapid-eye-movement (REM) as well as quiet (QS) sleep; phasic increases in SM EMG were similar during REM and QS occlusions in the majority (16/22) of babies. Periods of airway closure were detected during 24 occlusions in 5 infants; phasic SM EMG was reduced on these occasions. The results are consistent with the idea that recruitment of upper airway muscles contributes to the stability of the airway of the preterm human.     

Inhibition of inspiratory upper airway motoneuron activity by phasic volume feedback

The effects of phasic volume feedback on efferent hypoglossal, recurrent laryngeal and phrenic nerve activity were studied in decerebrate, paralyzed intubated cats ventilated with a phrenic-driven servo-respirator. The gain of the respirator was altered for single inspirations, and the resulting changes in neural activities were quantified by comparison with respective neural activities without phasic volume feedback. The volume thresholds for suppression of hypoglossal and recurrent laryngeal activities were time independent. Above these two thresholds and extending over a substantial range, volume feedback caused graded inhibition of upper airway motoneuron outputs. At any particular time during inspiration the relationships between hypoglossal or recurrent laryngeal inhibition and volume were concave to the volume axis. Rate of airflow appeared to exert an effect on upper airway motoneuron activity independent of volume. These results indicate that for hypoglossal and recurrent laryngeal efferent activity 1) volume feedback can cause a sustained graded inhibition throughout inspiration; 2) the volume thresholds are time independent; and 3) partial inhibition decreases susceptibility to additional inhibition. These actions of volume feedback on upper airway motoneuron output differ from those on phrenic efferent discharge and show that phasic vagal volume feedback has a marked and differential effect on upper airway motoneuron activity. The vagus, in this preparation, appears to play a critical role in the regulation of upper airway motoneuron activity and therefore maintenance of upper airway patency.     

Influence of muscle activity on the elastance of the upper airway of rabbits

This study sought to assess the effect of variations in upper airway muscle activity on upper airway pressure-volume properties. Upper airway elastance, closing pressure, and reserve volume were measured in the isolated upper airways of anesthetized rabbits under control conditions and after administration of gallamine (2 mg/kg iv) or after 10 min of spontaneous respiration of 7% CO2 in O2. Administration of gallamine to seven animals was associated with a fall in reserve volume from 0.94 +/- 0.24 to 0.69 +/- 0.17 (95% confidence interval) ml (P less than 0.01) and of closing pressure from -7.53 +/- 0.23 to -5.75 +/- 1.05 cmH2O (P less than 0.01), but airway elastance did not change significantly. Hypercapnia in seven animals was associated with a rise in elastance from 7.06 +/- 0.91 to 7.67 +/- 0.86 cmH2O/ml (P less than 0.001) and in reserve volume from 0.68 +/- 0.06 to 0.86 +/- 0.13 ml (P less than 0.05). Closing pressure also changed from -5.88 +/- 0.94 to -7.92 +/- 1.85 cmH2O. This change was correlated with the change in reserve volume but not with the change in elastance. In three animals exposed to hypercapnia, return to room air breathing was associated with return of elastance, reserve volume, and closing pressure to control levels. It is concluded that muscle activity in the upper airway affects both the size and elastance of the airway, but the dominant mechanism by which upper airway muscles increase the resistance of the upper airway to collapse is by increasing airway volume.     

Time of application of negative pressure pulses and upper airway muscle activity

Effect of upper airway pressure changes on thoracic inspiratory muscles has been shown to depend on the time of application during the breathing cycle. The present study was designed to investigate the importance of the time of application of upper airway negative pressure pulses on upper airway muscles. The upper airway was functionally isolated into a closed system in 24 anesthetized spontaneously breathing rabbits. Negative pressure pulses were applied in early (within the first 200 ms) and late (greater than or equal to 200 ms) inspiration, while electromyograms (EMG) of the diaphragm (Dia), genioglossus (GG), alae nasi (AN), and/or posterior cricoarytenoid (PCA) muscles were simultaneously monitored. When negative pressure pulse was applied in early inspiration, the increase in GG activity was greater [0.49 +/- 0.37 to 4.24 +/- 3.71 arbitrary units (AU)] than when negative pressure was applied in late inspiration (0.44 +/- 0.29 to 2.64 +/- 3.05 AU). Similarly, increased activation of AN (2.63 +/- 1.01 to 4.26 +/- 1.69 AU) and PCA (3.46 +/- 1.16 to 6.18 +/- 2.93 AU) was also observed with early inspiratory application of negative pressure pulses; minimal effects were seen in these muscles with late application. An inhibitory effect on respiratory timing consisting of a prolongation in inspiration (TI) and a decrease in peak Dia EMG/TI was observed as previously reported. These results indicate that the time of application of negative pressure during the breathing cycle is an important variable in determining the magnitude of the response of upper airway muscles.(ABSTRACT TRUNCATED AT 250 WORDS)     

Upper airway muscle paralysis reduces reflex upper airway motor response to negative transmural pressure in rat.

The reflex upper airway (UA) motor response to UA negative pressure (UANP) is attenuated by neuromuscular blockade. We hypothesized that this is due to a reduction in the sensitivity of laryngeal mechanoreceptors to changes in UA pressure. We examined the effect of neuromuscular blockade on hypoglossal motor responses to UANP and to asphyxia in 15 anesthetized, thoracotomized, artificially ventilated rats. The activity of laryngeal mechanoreceptors is influenced by contractions of laryngeal and tongue muscles, so we studied the effect of selective denervation of these muscle groups on the UA motor response to UANP and to asphyxia, recording from the pharyngeal branch of the glossopharyngeal nerve (n = 11). We also examined the effect of tongue and laryngeal muscle denervation on superior laryngeal nerve (SLN) afferent activity at different airway transmural pressures (n = 6). Neuromuscular blockade and denervation of laryngeal and tongue muscles significantly reduced baseline UA motor nerve activity (P < 0.05), caused a small but significant attenuation of the motor response to asphyxia, and markedly attenuated the response to UANP. Motor denervation of tongue and laryngeal muscles significantly decreased SLN afferent activity and altered the response to UANP. We conclude that skeletal muscle relaxation reduces the reflex UA motor response to UANP, and this may be due to a reduction in the excitability of UA motor systems as well as a decrease of the response of SLN afferents to UANP.