Physiology of Breathing and Respiratory Control during Sleep

William R. Krimsky; James C. Leiter

doi:10.1055/s-2005-864197

Seminars in Respiratory and Critical Care Medicine, Inhaltsverzeichnis

Semin Respir Crit Care Med 2005; 26(1): 5-12
DOI: 10.1055/s-2005-864197

Physiology of Breathing and Respiratory Control during Sleep

William R. Krimsky¹ , James C. Leiter¹ ^, ²

¹Departments of Medicine
²Physiology, Dartmouth Medical School, Lebanon, New Hampshire

Abstract

ABSTRACT

Studies of respiratory control during sleep have revealed that multiple sites of central CO₂ chemosensitivity exist within the brainstem, and different chemosensory sites may function only during certain sleep states. In general, chemical control of respiratory function, related to both hypercapnia and hypoxia, appears to be blunted during sleep. The decline in respiratory activity during sleep is particularly marked in the muscles of the upper airway. A variety of neuromechanical factors originating in the lungs, chest wall, and upper airway also modify respiratory function during sleep. Cardiorespiratory function seems to be less stable during sleep, and arousal responses represent a final element in the control system that preserves cardiorespiratory function by terminating the sleep state and restoring more effective control mechanisms.

KEYWORDS

Hypercapnia - hypoxia - upper airway reflexes - NREM sleep - REM sleep

Volltext

Referenzen

REFERENCES

1 Krueger J M, Obál F. Function of sleep. In: Lee-Chiong TL, Sateia MJ, Carskadon MA Sleep Medicine Philadelphia; Hanley & Belfus, Inc. 2002: 23-30
2 Kryger M H, Roth T, Dement W C. Principles and Practice of Sleep Medicine. Philadelphia, PA; Saunders 1995
3 Berthon-Jones M, Sullivan C E. Ventilation and arousal responses to hypercapnia in normal sleeping humans. J Appl Physiol. 1984; 57 59-67
4 Johnson M W, Remmers J E. Accessory muscle activity during sleep in chronic obstructive pulmonary disease. J Appl Physiol. 1984; 57 1011-1017
5 Rist K E, Daubenspeck J A, McGovern J F. Effects of non-REM sleep upon respiratory drive and the respiratory pump in humans. Respir Physiol. 1986; 63 241-256
6 Gervasoni D, Peyron C, Rampon C et al.. Role and origin of GABAergic innervation of dorsal raphe serotonergic neurons. J Neurosci. 2000; 20 4217-4225
7 Gallopian T, Fort P, Eggerman E et al.. Identification of sleep-promoting neurons in vitro. Nature. 2000; 404 992-995
8 Joseph V, Pequignot J M, Van Reeth O. Neurochemical perspectives on the control of breathing during sleep. Respir Physiol Neurobiol. 2002; 130 253-263
9 Nattie E E. Central chemosensitivity, sleep, and wakefulness. Respir Physiol. 2001; 129 257-268
10 Nattie E E. Multiple sites for central chemoreception: their roles in response sensitivity and in sleep and wakefulness. Respir Physiol. 2000; 122 223-235
11 Nattie E E, Li A. CO₂ dialysis in nucleus tractus solitarius region of rat increases ventilation in sleep and wakefulness. J Appl Physiol. 2002; 92 2119-2130
12 Parisian K, Wages P, Hewitt A, Leiter J C, Erlichman J S. Ventilatory effects of gap junction blockade in the NTS in awake rats. Respir Physiol Neurobiol. 2004; 142 127-143
13 Manning H L, Leiter J C. Respiratory control and respiratory sensation in a patient with a ganglioma within the dorsocaudal brain stem. Am J Respir Crit Care Med. 2000; 161 2100-2106
14 Morrell M J, Heywood P, Moosavi S H, Guz A, Stevens J. Unilateral focal lesions in the rostro-lateral medulla influence chemosensitivity and breathing during wakefulness, sleep, and exercise. J Neurol Neurosurg Psychiatry. 1998; 67 637-645
15 Akilesh M R, Kamper M, Li A, Nattie E E. Effects of unilateral lesion of retrotrapezoid nucleus on breathing in awake rats. J Appl Physiol. 1997; 82 469-479
16 Nattie E E, Li A. CO₂ dialysis in the medullary raphe of the rat increases ventilation in sleep. J Appl Physiol. 2001; 90 1247-1257
17 Curran A K, Darnall R A, Filiano J J, Li A, Nattie E E. Muscimol dialysis in the rostral ventral medulla reduces the ventilatory response to CO₂ in awake and sleeping piglets. J Appl Physiol. 2001; 90 971-980
18 Messier M L, Li A, Nattie E E. Muscimol inhibition of medullary raphé neurons decreases the CO₂ response and alters sleep in newborn piglets. Respir Physiol Neurobiol. 2002; 133 197-214
19 Dempsey J A, Smith C A, Harms C A, Chow C, Saupe K W. Sleep-induced breathing instability. Sleep. 1996; 19 236-247
20 Wang W, Bradley S R, Richerson G B. Quantification of the response of rat medullary raphe neurones to independent changes in pH_o and P_CO2 . J Physiol (Lond). 2002; 540 951-970
21 Filosa J A, Dean J B, Putnam R W. Role of intracellular and extracellular pH in the chemosensitive response of rat locus coeruleus neurones. J Physiol (Lond). 2002; 541 493-509
22 Erlichman J S, Cook A, Schwab M C, Budd T W, Leiter J C. Heterogeneous patterns of pH regulation in glial cells in the dorsal and ventral medulla. Am J Physiol. 2004; 286 R289-302
23 Nottingham S, Leiter J C, Wages P, Buhay S, Erlichman J S. Developmental changes in intracellular pH regulation in medullary neurons of the rat. Am J Physiol. 2001; 281 R1940-1951
24 Ritucci N A, Chambers-Kersh L, Dean J B, Putnam R W. Intracellular pH regulation in neurons from chemosensitive and nonchemosensitive areas of the medulla. Am J Physiol. 1998; 275 R1152-R1163
25 Prabhakar N R, Peng Y J. Peripheral chemoreceptors in health and disease. J Appl Physiol. 2004; 96 359-366
26 Pan L G, Forster H V, Martino P et al.. Important role of carotid afferents in control of breathing. J Appl Physiol. 1998; 85 1299-1306
27 Forster H V. Plasticity in the control of breathing following sensory denervation. J Appl Physiol. 2003; 94 784-794
28 Golanov E V, Ruggiero D A, Reis D J. A brainstem area mediating cerebrovascular and EEG responses to hypoxic excitation of rostral ventrolateral medulla in rat. J Physiol (Lond). 2000; 529 413-429
29 Solomon I C, Edelman N H, Neubauer J A. Pre-Bötzinger complex function as a central hypoxic chemosensor for respiration in vivo. J Neurophysiol. 2000; 83 2854-2868
30 Teppema L J, Veening J G, Kranenburg A, Dahan A, Berkenbosch A, Olievier C. Expression of c-fos in the rat brainstem after exposure to hypoxia and to normoxic and hyperoxic hypercapnia. J Comp Neurol. 1997; 388 169-190
31 Gozal D, Gaultier C. Evolving concepts of the maturation of central pathways underlying the hypoxic ventilatory response. Am J Respir Crit Care Med. 2001; 164 325-329
32 Gargaglioni L H, Coimbra N C, Branco L GS. The nucleus raphe magnus modulates hypoxia-induced hyperventilation but not anapyrexia in rats. Neurosci Lett. 2003; 347 121-125
33 Lovering A T, Dunin-Barkowski W L, Vidruk E H, Orem J M. Ventilatory response of the cat to hypoxia in sleep and wakefulness. J Appl Physiol. 2003; 95 545-554
34 Berthon-Jones M, Sullivan C E. Ventilatory and arousal responses to hypoxia in sleeping humans. Am Rev Respir Dis. 1982; 125 632-639
35 Douglas N J, White D P, Weil J V et al.. Hypoxic ventilatory response decreases during sleep in normal men. Am Rev Respir Dis. 1982; 125 286-289
36 Hedemark L L, Kronenberg R S. Ventilatory and heart responses to hypoxia and hypercapnia during sleep in adults. J Appl Physiol. 1982; 53 307-312
37 White D P, Douglas N J, Pickett C K, Weil J V, Zwillich C W. Hypoxic ventilatory response during sleep in normal premenopausal women. Am Rev Respir Dis. 1982; 126 530-533
38 Darnall R A, Curran A K, Filiano J J, Li A, Nattie E E. The effects of GABA_A agonist in the rostral ventral medulla on sleep and breathing in newborn piglets. Sleep. 2001; 24 514-527
39 Berry R B, Gleeson K. Respiratory arousal from sleep: mechanisms and significance. Sleep. 1997; 20 654-675
40 Sanders M H, Costantino J P, Owens G R et al.. Breathing during wakefulness and sleep after human heart-lung transplantation. Am Rev Respir Dis. 1989; 140 45-51
41 Sciurba F C, Owens G R, Sanders M H et al.. Evidence of an altered pattern of breathing during exercise in recipients of heart-lung transplants. N Engl J Med. 1988; 319 1186-1192
42 Kagawa F T, Duncan S R, Theodore J. Inspiratory timing of heart-lung transplant recipients during progressive hypercapnia. J Appl Physiol. 1991; 71 945-950
43 Henke K G, Arias A, Skatrud J B, Dempsey J A. Inhibition of inspiratory muscle activity during sleep: chemical and nonchemical influences. Am Rev Respir Dis. 1988; 138 8-15
44 Simon P M, Dempsey J A, Landry D M, Skatrud J B. Effect of sleep on respiratory muscle activity during mechanical ventilation. Am Rev Respir Dis. 1993; 147 32-37
45 BuSha B F, Stella M H, Manning H L, Leiter J C. Termination of inspiration by phase-dependent respiratory vagal feedback in awake normal humans. J Appl Physiol. 2002; 93 903-910
46 BuSha B, Judd B, Manning H L et al.. Identification of respiratory vagal feedback in awake normal subjects using pseudo-random unloading. J Appl Physiol. 2001; 90 2330-2340
47 Iber C, Simon P, Skatrud J B, Mahowald M W, Dempsey J A. The Breuer-Hering reflex in humans. Am J Respir Crit Care Med. 1995; 152 217-224
48 Simon P M, Habel A M, Daubenspeck J A, Leiter J C. Vagal feedback in the entrainment of respiration to mechanical ventilation in sleeping humans. J Appl Physiol. 2000; 89 760-769
49 Bakers J HCM, Tenney S M. The perception of some sensations associated with breathing. Respir Physiol. 1970; 10 85-92
50 Bartlett Jr D, St. John W M. Influence of lung volume on phrenic, hypoglossal and mylohyoid nerve activities. Respir Physiol. 1988; 73 97-110
51 Kuna S T. Inhibition of inspiratory upper airway motoneuron activity by phasic volume feedback. J Appl Physiol. 1986; 60 1373-1379
52 Wilson C R, Satoh M, Skatrud J B, Dempsey J A. Non-chemical inhibition of respiratory motor output during mechanical ventilation in sleeping humans. J Physiol. 1999; 518 605-618
53 Pillar G, Malhotra A, Fogel R B et al.. Upper airway muscle responsiveness to rising PCO₂ during NREM sleep. J Appl Physiol. 2000; 89 1275-1282
54 Horner R L, Liu X, Gill H, Nolan P, Liu H, Sood S. Effects of sleep-wake state on the genioglossus vs. diaphragm muscle responses in CO₂ in rats. J Appl Physiol. 2002; 92 878-887
55 Parisi R A, Santiago T V, Edelman N H. Genioglossal and diaphragm EMG responses to hypoxia druing sleep. Am Rev Respir Dis. 1988; 138 610-616
56 Schneider H, Boudewyns A, Smith P L et al.. Modulation of upper airway collapsibility during sleep: influence of respiratory phase and flow regimen. J Appl Physiol. 2002; 93 1365-1376
57 Basner R C, Ringler J, Berkowitz S et al.. Effect of inspired air temperature on genioglossus activity during nose breathing in awake humans. J Appl Physiol. 1990; 69 1098-1103
58 Basner R C, Simon P M, Schwartzstein R M, Weinberger S E, Weiss J W. Breathing route influences upper airway muscle activity in awake normal adults. J Appl Physiol. 1989; 66 1766-1771
59 Kimoff R J, Sforza E, Champagne L, Ofiara L, Gendron D. Upper airway sensation in snoring and obstructive sleep apnea. Am J Respir Crit Care Med. 2001; 164 250-255
60 Larsson H, Carlsson-Nordlander B, Lindblad L E, Norbeck O, Svanberg E. Temperature thresholds in the oropharynx of patients with obstructive sleep apnea syndrome. Am Rev Respir Dis. 1992; 146 1246-1249
61 Akay M, Leiter J C, Daubenspeck J A. Reduced respiratory-related evoked activity in subjects with obstructive sleep apnea syndrome. J Appl Physiol. 2003; 94 429-438
62 Afifi L, Guilleminault C, Colrain I M. Sleep and respiratory specific dampening of cortical responsivenss in OSAS. Respir Physiol Neurobiol. 2003; 136 221-234
63 Henke K G, Badr M S, Skatrud J B, Dempsey J A. Load compensation and respiratory muscle function during sleep. J Appl Physiol. 1992; 72 1221-1234
64 Wiegand D A, Latz B, Zwillich C W, Wiegand L. Upper airway resistance and geniohyoid muscle activity in normal men during wakefulness and sleep. J Appl Physiol. 1990; 69 1252-1261
65 Henke K G, Dempsey J A, Kowitz J M, Skatrud J B. Effects of sleep-induced increases in upper airway resistance on ventilation. J Appl Physiol. 1990; 69 617-624
66 Wiegand L, Zwillich C, White D P. Collapsibility of the human upper airway during normal sleep. J Appl Physiol. 1989; 66 1800-1808
67 Milic-Emili J, Tyler J M. Relation between work output of respiratory muscles and end-tidal CO₂ tension. J Appl Physiol. 1963; 18 497-504
68 Hendricks J C, Kline L R, Kovalski R J, O'Brien J A, Morrison A R, Pack A I. The English bulldog: a natural model of sleep-disordered breathing. J Appl Physiol. 1987; 63 1344-1350
69 Negus V E. The Comparative Anatomy and Physiology of the Larynx. London; W. Heinemann Medical Books 1949
70 Tuck S A, Dort J C, Olson M E, Remmers J E. Monitoring respiratory function and sleep in the obses Vietnamese pot-bellied pig. J Appl Physiol. 1999; 87 444-451

James C LeiterM.D.

Department of Medicine, Dartmouth Medical School

One Medical Center Dr., Lebanon, NH 03756

eMail: james.c.leiter@dartmouth.edu