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Control of Breathing During Sleep

Eliot A. Phillipson, Glenn Bowes

10.1002/cphy.cp030219

Source: Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing

Originally published: 1986

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Sleep‐Wakefulness States
1.1 Identification and Organization
1.2 Mechanisms and Functions
2 Central Neuronal Sleep‐Respiratory Interactions
3 Respiratory Muscle Function
3.1 General Concepts
3.2 Diaphragm and Intercostal Muscles
3.3 Upper Airway Muscles
4 Ventilation and Gas Exchange
4.1 NREM Sleep
4.2 REM Sleep
5 Pattern of Breathing
5.1 NREM Sleep
5.2 REM Sleep
6 Ventilatory Responses to Respiratory Stimuli
6.1 Response to CO2
6.2 Response to Hypoxia
6.3 Response to Upper Airway Stimulation
6.4 Response to Bronchopulmonary Stimulation
6.5 Response to Chest Wall Stimulation
6.6 Response to Thermal Stimuli
7 Arousal Responses to Respiratory Stimuli
7.1 Arousal Thresholds
7.2 Mechanisms of Arousal
7.3 Physiological Importance
Figure 1. Figure 1.

Recorder tracings in healthy adolescent demonstrating differences in chest wall mechanics between non‐rapid‐eye‐movement (NON‐REM) and rapid‐eye‐movement (REM) sleep. EMG I and EMG D, electromyograms of external intercostal and diaphragm, respectively; MTA I and MTA D, moving‐time averages of intercostal and diaphragmatic EMG, respectively; RC and ABD, volume change of rib cage and abdomen, respectively; VT, tidal volume. Note that during REM sleep intercostal muscle activity and rib cage contribution to Vt are decreased; Vt is maintained by increase in diaphragmatic activity.

From Tabachnik et al. 277
Figure 2. Figure 2.

Recorder tracings in healthy subject demonstrating effect of sleep‐wakefulness state on genioglossal muscle activity. EEG, electroencephalogram; EYE MOV, eye movements; CHIN and GEN EMG, chin and genioglossal electromyograms; RESP, respiratory movements. Note continuous discharge of GEN EMG, with inspiratory augmentation during waking and quiet (non‐rapid‐eye‐movement) sleep. In contrast, during rapid‐eye‐movement (REM) sleep genioglossal activity ceases except for small bursts during inspiration. Calibration: time, 1‐s intervals; amplitude, 50 μV.

From Sauerland and Harper 250
Figure 3. Figure 3.

Four possible mechanisms (dashed lines) by which sleep processes could interact with elements of the respiratory control system. and , partial pressures of O2 and CO2, respectively.
Figure 4. Figure 4.

Mechanisms underlying periodic breathing during stages 1 and 2 of non‐rapid‐eye‐movement sleep at sea level (A) and at high altitude (B). , minute volume of alveolar ventilation; and , arterial partial pressures of CO2 and O2, respectively. Line 1, changes in and resulting from spontaneous changes in at fixed rate of CO2 production. Line 2, ventilatory response to CO2 during wakefulness. Line 3, ventilatory response to hypoxia during wakefulness. A: As sleep ensues, decreases from a to b, resulting in small increase in and decrease in . With arousal, present at b now represents hypercapnic stimulus to breathing and drives to c, which represents demanded during wakefulness by that . With increase in , decreases, and and return from c to a. As level of wakefulness again decreases, cycle repeats, and oscillates from a to b to c to a until steady level of sleep develops. The present during sleep (b) would elicit only a minimal increase in to d when arousal occurs. Thus under normoxic conditions periodic breathing during sleep is not induced by these small changes in nor abolished by administration of O2. B: with onset of sleep, again decreases from a to b. With arousal, present at b would drive only to c, whereas present at b drives to d, which represents demanded during wakefulness by that . Thus under hypoxic conditions periodic breathing during sleep is induced by small change in resulting from sleep and is therefore reduced or abolished by administration of O2.

From Phillipson 211
Figure 5. Figure 5.

Number of episodes of regular breathing during sleep (measured at 5‐min intervals) as function of time from onset of sleep in 14 healthy subjects.

Adapted from Magnussen 158
Figure 6. Figure 6.

Minute‐by‐minute fluctuations in cardiorespiratory variables during 100 min of uninterrupted sleep in healthy subject. EM, eye movements; EEG, electroencephalogram; SBP, systolic blood pressure; RESP, respiratory frequency; PULSE, heart rate; BM, body movements. Note that during rapid‐eye‐movement sleep (242–273 min), two sustained bursts of eye movements (indicated by filled bars) were associated with marked irregularities in SBP, RESP, and PULSE.

From Snyder et al. 263
Figure 7. Figure 7.

Recorder tracings in sleeping dog demonstrating differences in pattern of breathing between phasic and tonic rapid‐eye‐movement sleep. V, inspired tidal volume (above zero line); , rate of airflow (inspiration upwards); EMG, nuchal muscle electromyogram. Initially dog was in phasic rapid‐eye‐movement sleep, indicated by suppression of tonic EMG activity but presence of irregular phasic EMG bursts. Note irregular pattern of breathing. First arrow, phasic rapid‐eye‐movement activity ceased, and breathing became more regular. Second arrow, dog awoke. Note return of tonic EMG activity.

From Phillipson 211
Figure 8. Figure 8.

Recorder tracings in sleeping dog demonstrating effects of cervical vagal blockade on pattern of breathing in slow‐wave sleep (SWS) and rapid‐eye‐movement (REM) sleep. Vi, inspired tidal volume (above zero line); , rate of airflow (inspiration upwards). Note vagal blockade failed to abolish irregularity of breathing pattern during REM sleep.

From Phillipson 210
Figure 9. Figure 9.

Recorder tracings in sleeping dog showing persistence of irregular pattern of breathing during rapid‐eye‐movement sleep despite progressive hypercapnia. CO2, concentration of CO2 in tracheal gas; V, inspired volume (above zero line); , rate of airflow (inspiration upwards); EEG, electroencephalogram. A, onset of phasic rapid‐eye‐movement sleep; B, onset of CO2 rebreathing; C, cessation of generalized muscular twitching; D, dog swallowing; E, arousal. Note irregular pattern of breathing during period of generalized muscular twitching and period of apnea during swallowing.

From Sullivan et al. 274
Figure 10. Figure 10.

Effects of non‐rapid‐eye‐movement sleep on mean ventilatory responses to CO2 in normal subjects. /BSA, minute volume of ventilation normalized for body surface area; S/Q, sensitivity quotient; , formula used to compare all slopes with one common reference mean slope; , alveolar CO2 pressure; Aα, alert wakefulness; A, quiet wakefulness; B, stage 1; C, stage 2; D, stage 3; E, stage 4. All lines have been scaled to common reference curve (line A). Note shift to higher levels and decrease in slope of response lines with progressively deeper stages of non‐rapid‐eye‐movement sleep.

From Bulow 34
Figure 11. Figure 11.

Breath‐by‐breath response of minute volume of ventilation (i) to decreasing arterial O2 saturation () and to increasing alveolar partial pressure of CO2 () in sleeping dog. •, Slow‐wave sleep; ○, rapid‐eye‐movement sleep. Note scatter of data points around calculated linear regression lines during rapid‐eye‐movement sleep and marked decrease in response to increasing .

From Phillipson 210
Figure 12. Figure 12.

Recorder tracings in sleeping dog demonstrating effect of sleep‐wakefulness state on responses to laryngeal stimulation. V, inspired volume (above zero line); , rate of airflow (inspiration upwards); EEG, electroencephalogram; ECG, electrocardiogram. Lowest trace, stimulus marker. During wakefulness (A), injection of 0.2 ml of water onto larynx caused coughing. During slow‐wave sleep (B), same stimulus elicited brief expiration reflex but no arousal or coughing. Larger stimulus (c) caused arousal from slow‐wave sleep (at arrow) followed by coughing. In contrast, during rapid‐eye‐movement sleep (D), same stimulus failed to produce arousal or coughing but did elicit transient bradycardia.

From Sullivan et al. 273
Figure 13. Figure 13.

Recorder tracings from sleeping cat demonstrating responses to airway occlusion during sleep. A: non‐rapid‐eye‐movement sleep. EEG, electroencephalogram; EMG, electromyogram; PCA, posterior cricoarytenoid. Occluded breaths are indicated by numbered fluctuations in intratracheal pressure. Note arousal from non‐rapid‐eye‐movement sleep after second occluded breath and progressive increases in diaphragmatic and PCA activity during airway occlusion. B: rapid‐eye‐movement (REM) sleep. INT, integrated; PGO waves, pontogeniculo‐occipital discharges. Note delayed arousal to airway occlusion during REM sleep compared with that during non‐rapid‐eye‐movement sleep and absence of progressive diaphragmatic response to airway occlusion.

From Orem et al. 190
Figure 14. Figure 14.

Recorder tracings in sleeping cat demonstrating differences in ventilatory response to thermal stimulus between slow‐wave sleep (A) and rapid‐eye‐movement sleep (B). P, O, and Hp, parietal, occipital, and hippocampus dorsalis discharges; EMG, nuchal muscle electromyogram; RM, respiratory movements. Note marked tachypnea during slow‐wave sleep in response to high environmental temperature and lack of tachypnea during rapid‐eye‐movement sleep despite same environmental temperature.

From Parmeggiani and Rabini 207
Figure 15. Figure 15.

Recorder tracings in sleeping dog demonstrating ventilatory and arousal responses to airway occlusion during non‐rapid‐eye‐movement sleep. A: intact. , arterial O2 saturation; Vt, tidal volume; , airflow rate (inspiration upwards); Ptr, tracheal pressure, EEG, electroencephalogram; a, onset of airway occlusion; b, movement arousal and termination of airway occlusion. B: same dog shown in A after bilateral carotid body denervation. Note delayed arousal response to airway occlusion compared with that in intact state (A), transient nature of arousal response, and impaired ventilatory response during airway occlusion. ECG, electrocardiogram.

From Bowes et al. 26


Figure 1.

Recorder tracings in healthy adolescent demonstrating differences in chest wall mechanics between non‐rapid‐eye‐movement (NON‐REM) and rapid‐eye‐movement (REM) sleep. EMG I and EMG D, electromyograms of external intercostal and diaphragm, respectively; MTA I and MTA D, moving‐time averages of intercostal and diaphragmatic EMG, respectively; RC and ABD, volume change of rib cage and abdomen, respectively; VT, tidal volume. Note that during REM sleep intercostal muscle activity and rib cage contribution to Vt are decreased; Vt is maintained by increase in diaphragmatic activity.

From Tabachnik et al. 277


Figure 2.

Recorder tracings in healthy subject demonstrating effect of sleep‐wakefulness state on genioglossal muscle activity. EEG, electroencephalogram; EYE MOV, eye movements; CHIN and GEN EMG, chin and genioglossal electromyograms; RESP, respiratory movements. Note continuous discharge of GEN EMG, with inspiratory augmentation during waking and quiet (non‐rapid‐eye‐movement) sleep. In contrast, during rapid‐eye‐movement (REM) sleep genioglossal activity ceases except for small bursts during inspiration. Calibration: time, 1‐s intervals; amplitude, 50 μV.

From Sauerland and Harper 250


Figure 3.

Four possible mechanisms (dashed lines) by which sleep processes could interact with elements of the respiratory control system. and , partial pressures of O2 and CO2, respectively.



Figure 4.

Mechanisms underlying periodic breathing during stages 1 and 2 of non‐rapid‐eye‐movement sleep at sea level (A) and at high altitude (B). , minute volume of alveolar ventilation; and , arterial partial pressures of CO2 and O2, respectively. Line 1, changes in and resulting from spontaneous changes in at fixed rate of CO2 production. Line 2, ventilatory response to CO2 during wakefulness. Line 3, ventilatory response to hypoxia during wakefulness. A: As sleep ensues, decreases from a to b, resulting in small increase in and decrease in . With arousal, present at b now represents hypercapnic stimulus to breathing and drives to c, which represents demanded during wakefulness by that . With increase in , decreases, and and return from c to a. As level of wakefulness again decreases, cycle repeats, and oscillates from a to b to c to a until steady level of sleep develops. The present during sleep (b) would elicit only a minimal increase in to d when arousal occurs. Thus under normoxic conditions periodic breathing during sleep is not induced by these small changes in nor abolished by administration of O2. B: with onset of sleep, again decreases from a to b. With arousal, present at b would drive only to c, whereas present at b drives to d, which represents demanded during wakefulness by that . Thus under hypoxic conditions periodic breathing during sleep is induced by small change in resulting from sleep and is therefore reduced or abolished by administration of O2.

From Phillipson 211


Figure 5.

Number of episodes of regular breathing during sleep (measured at 5‐min intervals) as function of time from onset of sleep in 14 healthy subjects.

Adapted from Magnussen 158


Figure 6.

Minute‐by‐minute fluctuations in cardiorespiratory variables during 100 min of uninterrupted sleep in healthy subject. EM, eye movements; EEG, electroencephalogram; SBP, systolic blood pressure; RESP, respiratory frequency; PULSE, heart rate; BM, body movements. Note that during rapid‐eye‐movement sleep (242–273 min), two sustained bursts of eye movements (indicated by filled bars) were associated with marked irregularities in SBP, RESP, and PULSE.

From Snyder et al. 263


Figure 7.

Recorder tracings in sleeping dog demonstrating differences in pattern of breathing between phasic and tonic rapid‐eye‐movement sleep. V, inspired tidal volume (above zero line); , rate of airflow (inspiration upwards); EMG, nuchal muscle electromyogram. Initially dog was in phasic rapid‐eye‐movement sleep, indicated by suppression of tonic EMG activity but presence of irregular phasic EMG bursts. Note irregular pattern of breathing. First arrow, phasic rapid‐eye‐movement activity ceased, and breathing became more regular. Second arrow, dog awoke. Note return of tonic EMG activity.

From Phillipson 211


Figure 8.

Recorder tracings in sleeping dog demonstrating effects of cervical vagal blockade on pattern of breathing in slow‐wave sleep (SWS) and rapid‐eye‐movement (REM) sleep. Vi, inspired tidal volume (above zero line); , rate of airflow (inspiration upwards). Note vagal blockade failed to abolish irregularity of breathing pattern during REM sleep.

From Phillipson 210


Figure 9.

Recorder tracings in sleeping dog showing persistence of irregular pattern of breathing during rapid‐eye‐movement sleep despite progressive hypercapnia. CO2, concentration of CO2 in tracheal gas; V, inspired volume (above zero line); , rate of airflow (inspiration upwards); EEG, electroencephalogram. A, onset of phasic rapid‐eye‐movement sleep; B, onset of CO2 rebreathing; C, cessation of generalized muscular twitching; D, dog swallowing; E, arousal. Note irregular pattern of breathing during period of generalized muscular twitching and period of apnea during swallowing.

From Sullivan et al. 274


Figure 10.

Effects of non‐rapid‐eye‐movement sleep on mean ventilatory responses to CO2 in normal subjects. /BSA, minute volume of ventilation normalized for body surface area; S/Q, sensitivity quotient; , formula used to compare all slopes with one common reference mean slope; , alveolar CO2 pressure; Aα, alert wakefulness; A, quiet wakefulness; B, stage 1; C, stage 2; D, stage 3; E, stage 4. All lines have been scaled to common reference curve (line A). Note shift to higher levels and decrease in slope of response lines with progressively deeper stages of non‐rapid‐eye‐movement sleep.

From Bulow 34


Figure 11.

Breath‐by‐breath response of minute volume of ventilation (i) to decreasing arterial O2 saturation () and to increasing alveolar partial pressure of CO2 () in sleeping dog. •, Slow‐wave sleep; ○, rapid‐eye‐movement sleep. Note scatter of data points around calculated linear regression lines during rapid‐eye‐movement sleep and marked decrease in response to increasing .

From Phillipson 210


Figure 12.

Recorder tracings in sleeping dog demonstrating effect of sleep‐wakefulness state on responses to laryngeal stimulation. V, inspired volume (above zero line); , rate of airflow (inspiration upwards); EEG, electroencephalogram; ECG, electrocardiogram. Lowest trace, stimulus marker. During wakefulness (A), injection of 0.2 ml of water onto larynx caused coughing. During slow‐wave sleep (B), same stimulus elicited brief expiration reflex but no arousal or coughing. Larger stimulus (c) caused arousal from slow‐wave sleep (at arrow) followed by coughing. In contrast, during rapid‐eye‐movement sleep (D), same stimulus failed to produce arousal or coughing but did elicit transient bradycardia.

From Sullivan et al. 273


Figure 13.

Recorder tracings from sleeping cat demonstrating responses to airway occlusion during sleep. A: non‐rapid‐eye‐movement sleep. EEG, electroencephalogram; EMG, electromyogram; PCA, posterior cricoarytenoid. Occluded breaths are indicated by numbered fluctuations in intratracheal pressure. Note arousal from non‐rapid‐eye‐movement sleep after second occluded breath and progressive increases in diaphragmatic and PCA activity during airway occlusion. B: rapid‐eye‐movement (REM) sleep. INT, integrated; PGO waves, pontogeniculo‐occipital discharges. Note delayed arousal to airway occlusion during REM sleep compared with that during non‐rapid‐eye‐movement sleep and absence of progressive diaphragmatic response to airway occlusion.

From Orem et al. 190


Figure 14.

Recorder tracings in sleeping cat demonstrating differences in ventilatory response to thermal stimulus between slow‐wave sleep (A) and rapid‐eye‐movement sleep (B). P, O, and Hp, parietal, occipital, and hippocampus dorsalis discharges; EMG, nuchal muscle electromyogram; RM, respiratory movements. Note marked tachypnea during slow‐wave sleep in response to high environmental temperature and lack of tachypnea during rapid‐eye‐movement sleep despite same environmental temperature.

From Parmeggiani and Rabini 207


Figure 15.

Recorder tracings in sleeping dog demonstrating ventilatory and arousal responses to airway occlusion during non‐rapid‐eye‐movement sleep. A: intact. , arterial O2 saturation; Vt, tidal volume; , airflow rate (inspiration upwards); Ptr, tracheal pressure, EEG, electroencephalogram; a, onset of airway occlusion; b, movement arousal and termination of airway occlusion. B: same dog shown in A after bilateral carotid body denervation. Note delayed arousal response to airway occlusion compared with that in intact state (A), transient nature of arousal response, and impaired ventilatory response during airway occlusion. ECG, electrocardiogram.

From Bowes et al. 26
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Article Title: Control of Breathing During Sleep
 

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Eliot A. Phillipson, Glenn Bowes. Control of Breathing During Sleep. Compr Physiol 2011, Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing: 649-689. First published in print 1986. doi: 10.1002/cphy.cp030219