Abstract
1. The influence of the upper airway on the ventilatory and arousal responses to hypercapnia in wakefulness and sleep was investigated using a chronic animal model. 2. Experiments were performed in five unrestrained dogs trained to sleep naturally in the laboratory. The animal rebreathed through a chronic tracheostoma (thus excluding the upper airway from the breathing circuit), or through the snout (intact upper airway). Resistance to breathing and volume of dead space during quiet tracheal breathing were matched to those in quiet nasal breathing during wakefulness and sleep. CO2 rebreathing tests were performed during wakefulness, rapid eye movement (REM) and non-REM (NREM) sleep, during nasal and tracheal breathing. 3. The ventilatory response to hypercapnia was significantly lower in nasal breathing compared with tracheal breathing, in all behavioural states. This was due to a smaller tidal volume and lower breathing frequency. 4. The ventilatory response to CO2 was lowest during REM sleep, irrespective of route used for breathing. 5. Alveolar partial pressure of CO2 (PA,CO2) level at arousal was identical in NREM nasal and tracheal rebreathing tests. Differences in PA,CO2 levels at arousal between NREM and REM sleep were not significant in nasal tests and only marginally different during tracheal breathing. 6. We conclude that nasal breathing influences the hypercapnic ventilatory response in wakefulness and sleep, and that the presence of CO2 in the upper airway does not affect arousal in NREM and REM sleep.
Full text
PDF













Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Badr M. S., Skatrud J. B., Simon P. M., Dempsey J. A. Effect of hypercapnia on total pulmonary resistance during wakefulness and during NREM sleep. Am Rev Respir Dis. 1991 Aug;144(2):406–414. doi: 10.1164/ajrccm/144.2.406. [DOI] [PubMed] [Google Scholar]
- Baker M. A., Chapman L. W., Nathanson M. Control of brain temperature in dogs: effects of tracheostomy. Respir Physiol. 1974 Dec;22(3):325–333. doi: 10.1016/0034-5687(74)90081-4. [DOI] [PubMed] [Google Scholar]
- Berthon-Jones M., Sullivan C. E. Ventilation and arousal responses to hypercapnia in normal sleeping humans. J Appl Physiol Respir Environ Exerc Physiol. 1984 Jul;57(1):59–67. doi: 10.1152/jappl.1984.57.1.59. [DOI] [PubMed] [Google Scholar]
- Berthon-Jones M., Sullivan C. E. Ventilatory and arousal responses to hypoxia in sleeping humans. Am Rev Respir Dis. 1982 Jun;125(6):632–639. doi: 10.1164/arrd.1982.125.6.632. [DOI] [PubMed] [Google Scholar]
- Boushey H. A., Richardson P. S. The reflex effects of intralaryngeal carbon dioxide on the pattern of breathing. J Physiol. 1973 Jan;228(1):181–191. doi: 10.1113/jphysiol.1973.sp010080. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bowes G., Townsend E. R., Kozar L. F., Bromley S. M., Phillipson E. A. Effect of carotid body denervation on arousal response to hypoxia in sleeping dogs. J Appl Physiol Respir Environ Exerc Physiol. 1981 Jul;51(1):40–45. doi: 10.1152/jappl.1981.51.1.40. [DOI] [PubMed] [Google Scholar]
- Burgess K. R., Whitelaw W. A. Reducing ventilatory response to carbon dioxide by breathing cold air. Am Rev Respir Dis. 1984 May;129(5):687–690. doi: 10.1164/arrd.1984.129.5.687. [DOI] [PubMed] [Google Scholar]
- Douglas N. J., White D. P., Weil J. V., Pickett C. K., Zwillich C. W. Hypercapnic ventilatory response in sleeping adults. Am Rev Respir Dis. 1982 Nov;126(5):758–762. doi: 10.1164/arrd.1982.126.5.758. [DOI] [PubMed] [Google Scholar]
- Douglas N. J., White D. P., Weil J. V., Zwillich C. W. Effect of breathing route on ventilation and ventilatory drive. Respir Physiol. 1983 Feb;51(2):209–218. doi: 10.1016/0034-5687(83)90041-5. [DOI] [PubMed] [Google Scholar]
- Gleeson K., Zwillich C. W., White D. P. The influence of increasing ventilatory effort on arousal from sleep. Am Rev Respir Dis. 1990 Aug;142(2):295–300. doi: 10.1164/ajrccm/142.2.295. [DOI] [PubMed] [Google Scholar]
- Goh A. S., Issa F. G., Sullivan C. E. Upper airway dilating forces during wakefulness and sleep in dogs. J Appl Physiol (1985) 1986 Dec;61(6):2148–2155. doi: 10.1152/jappl.1986.61.6.2148. [DOI] [PubMed] [Google Scholar]
- Gothe B., Altose M. D., Goldman M. D., Cherniack N. S. Effect of quiet sleep on resting and CO2-stimulated breathing in humans. J Appl Physiol Respir Environ Exerc Physiol. 1981 Apr;50(4):724–730. doi: 10.1152/jappl.1981.50.4.724. [DOI] [PubMed] [Google Scholar]
- Hales J. R., Bligh J. Respiratory responses of the conscious dog to severe heat stress. Experientia. 1969 Aug 15;25(8):818–819. doi: 10.1007/BF01897895. [DOI] [PubMed] [Google Scholar]
- Hedemark L. L., Kronenberg R. S. Ventilatory and heart rate responses to hypoxia and hypercapnia during sleep in adults. J Appl Physiol Respir Environ Exerc Physiol. 1982 Aug;53(2):307–312. doi: 10.1152/jappl.1982.53.2.307. [DOI] [PubMed] [Google Scholar]
- Horner R. L., Innes J. A., Holden H. B., Guz A. Afferent pathway(s) for pharyngeal dilator reflex to negative pressure in man: a study using upper airway anaesthesia. J Physiol. 1991 May;436:31–44. doi: 10.1113/jphysiol.1991.sp018537. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horner R. L., Innes J. A., Murphy K., Guz A. Evidence for reflex upper airway dilator muscle activation by sudden negative airway pressure in man. J Physiol. 1991 May;436:15–29. doi: 10.1113/jphysiol.1991.sp018536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Issa F. G., Edwards P., Szeto E., Lauff D., Sullivan C. Genioglossus and breathing responses to airway occlusion: effect of sleep and route of occlusion. J Appl Physiol (1985) 1988 Feb;64(2):543–549. doi: 10.1152/jappl.1988.64.2.543. [DOI] [PubMed] [Google Scholar]
- Issa F. G., McNamara S. G., Sullivan C. E. Arousal responses to airway occlusion in sleeping dogs: comparison of nasal and tracheal occlusions. J Appl Physiol (1985) 1987 May;62(5):1832–1836. doi: 10.1152/jappl.1987.62.5.1832. [DOI] [PubMed] [Google Scholar]
- Issa F. G., Sullivan C. E. Arousal and breathing responses to airway occlusion in healthy sleeping adults. J Appl Physiol Respir Environ Exerc Physiol. 1983 Oct;55(4):1113–1119. doi: 10.1152/jappl.1983.55.4.1113. [DOI] [PubMed] [Google Scholar]
- Jammes Y., Davies A., Widdicombe J. G. Tracheobronchial and laryngeal responses to hypercapnia, histamine and capsaicin in dogs. Bull Eur Physiopathol Respir. 1985 Nov-Dec;21(6):515–520. [PubMed] [Google Scholar]
- Krabill V. A., Ghoshal N. G. Effect of tracheal by-pass on brain temperature and cerebrospinal fluid pressure in sheep. Zentralbl Veterinarmed A. 1983 Aug;30(7):542–551. doi: 10.1111/j.1439-0442.1983.tb01016.x. [DOI] [PubMed] [Google Scholar]
- Laburn H. P., Mitchell D., Mitchell G., Saffy K. Effects of tracheostomy breathing on brain and body temperatures in hyperthermic sheep. J Physiol. 1988 Dec;406:331–344. doi: 10.1113/jphysiol.1988.sp017383. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee L. Y., Morton R. F., McIntosh M. J., Turbek J. A. An isolated upper airway preparation in conscious dogs. J Appl Physiol (1985) 1986 Jun;60(6):2123–2127. doi: 10.1152/jappl.1986.60.6.2123. [DOI] [PubMed] [Google Scholar]
- Lydic R., Baghdoyan H. A., Wertz R., White D. P. Cholinergic reticular mechanisms influence state-dependent ventilatory response to hypercapnia. Am J Physiol. 1991 Sep;261(3 Pt 2):R738–R746. doi: 10.1152/ajpregu.1991.261.3.R738. [DOI] [PubMed] [Google Scholar]
- Maskrey M. Body temperature effects on hypoxic and hypercapnic responses in awake rats. Am J Physiol. 1990 Sep;259(3 Pt 2):R492–R498. doi: 10.1152/ajpregu.1990.259.3.R492. [DOI] [PubMed] [Google Scholar]
- Mathew O. P., Abu-Osba Y. K., Thach B. T. Influence of upper airway pressure changes on respiratory frequency. Respir Physiol. 1982 Aug;49(2):223–233. doi: 10.1016/0034-5687(82)90075-5. [DOI] [PubMed] [Google Scholar]
- McCaffrey T. V., Kern E. B. Response of nasal airway resistance to hypercapnia and hypoxia in the dog. Acta Otolaryngol. 1979 May-Jun;87(5-6):545–553. doi: 10.3109/00016487909126463. [DOI] [PubMed] [Google Scholar]
- McNamara S. G., Issa F. G., Szeto E., Sullivan C. E. Influence of negative pressure applied to the upper airway on the breathing pattern in unanesthetized awake dogs. Respir Physiol. 1986 Sep;65(3):315–329. doi: 10.1016/0034-5687(86)90016-2. [DOI] [PubMed] [Google Scholar]
- NADEL J. A., WIDDICOMBE J. G. Effect of changes in blood gas tensions and carotid sinus pressure on tracheal volume and total lung resistance to airflow. J Physiol. 1962 Aug;163:13–33. doi: 10.1113/jphysiol.1962.sp006956. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parisi R. A., Neubauer J. A., Frank M. M., Santiago T. V., Edelman N. H. Linkage between brain blood flow and respiratory drive during rapid-eye-movement sleep. J Appl Physiol (1985) 1988 Apr;64(4):1457–1465. doi: 10.1152/jappl.1988.64.4.1457. [DOI] [PubMed] [Google Scholar]
- Phillipson E. A., Kozar L. F., Rebuck A. S., Murphy E. Ventilatory and waking responses to CO2 in sleeping dogs. Am Rev Respir Dis. 1977 Feb;115(2):251–259. doi: 10.1164/arrd.1977.115.2.251. [DOI] [PubMed] [Google Scholar]
- Phillipson E. A., Murphy E., Kozar L. F. Regulation of respiration in sleeping dogs. J Appl Physiol. 1976 May;40(5):688–693. doi: 10.1152/jappl.1976.40.5.688. [DOI] [PubMed] [Google Scholar]
- Plowman L., Lauff D. C., Berthon-Jones M., Sullivan C. E. Abdominal muscle activity in conscious dogs: effect of sleep and route of breathing. Respir Physiol. 1990 Sep;81(3):321–335. doi: 10.1016/0034-5687(90)90113-d. [DOI] [PubMed] [Google Scholar]
- Read D. J. A clinical method for assessing the ventilatory response to carbon dioxide. Australas Ann Med. 1967 Feb;16(1):20–32. doi: 10.1111/imj.1967.16.1.20. [DOI] [PubMed] [Google Scholar]
- Sant'Ambrogio G. Information arising from the tracheobronchial tree of mammals. Physiol Rev. 1982 Apr;62(2):531–569. doi: 10.1152/physrev.1982.62.2.531. [DOI] [PubMed] [Google Scholar]
- Sant'Ambrogio G., Mathew O. P., Fisher J. T., Sant'Ambrogio F. B. Laryngeal receptors responding to transmural pressure, airflow and local muscle activity. Respir Physiol. 1983 Dec;54(3):317–330. doi: 10.1016/0034-5687(83)90075-0. [DOI] [PubMed] [Google Scholar]
- Sant'Ambrogio G., Mathew O. P., Sant'Ambrogio F. B., Fisher J. T. Laryngeal cold receptors. Respir Physiol. 1985 Jan;59(1):35–44. doi: 10.1016/0034-5687(85)90016-7. [DOI] [PubMed] [Google Scholar]
- Skatrud J. B., Dempsey J. A., Badr S., Begle R. L. Effect of airway impedance on CO2 retention and respiratory muscle activity during NREM sleep. J Appl Physiol (1985) 1988 Oct;65(4):1676–1685. doi: 10.1152/jappl.1988.65.4.1676. [DOI] [PubMed] [Google Scholar]
- Sériès F., Cormier Y., Desmeules M., La Forge J. Influence of respiratory drive on upper airway resistance in normal men. J Appl Physiol (1985) 1989 Mar;66(3):1242–1249. doi: 10.1152/jappl.1989.66.3.1242. [DOI] [PubMed] [Google Scholar]
- Takagi Y., Proctor D. F., Salman S., Evering S. Effects of cold air and carbon dioxide on nasal air flow resistance. Ann Otol Rhinol Laryngol. 1969 Feb;78(1):40–48. doi: 10.1177/000348946907800104. [DOI] [PubMed] [Google Scholar]
- Tanaka Y., Morikawa T., Honda Y. An assessment of nasal functions in control of breathing. J Appl Physiol (1985) 1988 Oct;65(4):1520–1524. doi: 10.1152/jappl.1988.65.4.1520. [DOI] [PubMed] [Google Scholar]
- Tsubone H. Nasal 'flow' receptors of the rat. Respir Physiol. 1989 Jan;75(1):51–64. doi: 10.1016/0034-5687(89)90086-8. [DOI] [PubMed] [Google Scholar]
- Vincken W., Guilleminault C., Silvestri L., Cosio M., Grassino A. Inspiratory muscle activity as a trigger causing the airways to open in obstructive sleep apnea. Am Rev Respir Dis. 1987 Feb;135(2):372–377. doi: 10.1164/arrd.1987.135.2.372. [DOI] [PubMed] [Google Scholar]
