An endogenous circadian rhythm of respiratory control in humans

Christina M. Spengler, Charles A. Czeisler, Steven Shea

Research output: Contribution to journalArticle

90 Citations (Scopus)

Abstract

1. Many physiological and behavioural functions have circadian rhythms - endogenous oscillations with a period of approximately 24 h that can occur even in the absence of sleep. We determined whether there is an endogenous circadian rhythm in breathing, metabolism and ventilatory chemosensitivity in humans. 2. Ten healthy, adult males were studied throughout 4 days in a stable laboratory environment. After two initial baseline days (16 h wakefulness plus 8 h sleep) that served to achieve a steady state, subjects were studied under constant behavioural and environmental conditions throughout 41 h of wakefulness. Ventilation, metabolism and the magnitude of the hypercapnic ventilatory response (HCVR) were measured every 2 h. Individuals' data were aligned according to circadian phase (core body temperature minimum; CBT(min)) and averaged. 3. In the group average data, there was a significant and large amplitude circadian variation in HCVR slope (average of ±0·4 1 min -1 mmHg-1; corresponding to ± 12·1% of 24 h mean), and a smaller amplitude rhythm in the HCVR x-axis intercept (average of ± 1·1 mmHg; ±2·1% of 24 h mean). 4. Despite a significant circadian variation in metabolism (±3·2% of 24 h mean), there were no detectable rhythms in tidal volume, respiratory frequency or ventilation. This small discrepancy between metabolism and ventilation led to a small but significant circadian variation in end-tidal P(CO2) (P(ET,CO2); ±0·6 mmHg; ±1·5% of 24 h mean). 5. The circadian minima of the group-averaged respiratory variables occurred 6-8 h earlier than CBT(min), suggesting that endogenous changes in CBT across the circadian cycle have less of an effect on respiration than equivalent experimentally induced changes in CBT. 6. Throughout these circadian changes, there were no correlations between HCVR parameters (slope or x-axis intercept) and either resting ventilation or resting P(ET,CO2). This suggests that ventilation and P(ET,CO2) are little influenced by central chemosensory respiratory control in awake humans even when at rest under constant environmental and behavioural conditions. 7. The characteristic change in P(ET,CO2) during non-rapid eye movement sleep was shown to be independent of circadian variations in P(ET,CO2), and probably reflects a change from predominantly behavioural to predominantly chemosensory respiratory control. 8. This study has documented the existence and magnitude of circadian variations in respiration and respiratory control in awake humans for the first time under constant behavioural and environmental conditions. These results provide unique insights into respiratory control in awake humans, and highlight the importance of considering the phase of the circadian cycle in studies of respiratory control.

Original languageEnglish (US)
Pages (from-to)683-694
Number of pages12
JournalJournal of Physiology
Volume526
Issue number3
StatePublished - 2000
Externally publishedYes

Fingerprint

Circadian Rhythm
Ventilation
Sleep
Respiration
Wakefulness
Tidal Volume
Eye Movements
Body Temperature

ASJC Scopus subject areas

  • Physiology

Cite this

An endogenous circadian rhythm of respiratory control in humans. / Spengler, Christina M.; Czeisler, Charles A.; Shea, Steven.

In: Journal of Physiology, Vol. 526, No. 3, 2000, p. 683-694.

Research output: Contribution to journalArticle

Spengler, CM, Czeisler, CA & Shea, S 2000, 'An endogenous circadian rhythm of respiratory control in humans', Journal of Physiology, vol. 526, no. 3, pp. 683-694.
Spengler, Christina M. ; Czeisler, Charles A. ; Shea, Steven. / An endogenous circadian rhythm of respiratory control in humans. In: Journal of Physiology. 2000 ; Vol. 526, No. 3. pp. 683-694.
@article{31d8f1cf44d5425e81f7163a27df1fa4,
title = "An endogenous circadian rhythm of respiratory control in humans",
abstract = "1. Many physiological and behavioural functions have circadian rhythms - endogenous oscillations with a period of approximately 24 h that can occur even in the absence of sleep. We determined whether there is an endogenous circadian rhythm in breathing, metabolism and ventilatory chemosensitivity in humans. 2. Ten healthy, adult males were studied throughout 4 days in a stable laboratory environment. After two initial baseline days (16 h wakefulness plus 8 h sleep) that served to achieve a steady state, subjects were studied under constant behavioural and environmental conditions throughout 41 h of wakefulness. Ventilation, metabolism and the magnitude of the hypercapnic ventilatory response (HCVR) were measured every 2 h. Individuals' data were aligned according to circadian phase (core body temperature minimum; CBT(min)) and averaged. 3. In the group average data, there was a significant and large amplitude circadian variation in HCVR slope (average of ±0·4 1 min -1 mmHg-1; corresponding to ± 12·1{\%} of 24 h mean), and a smaller amplitude rhythm in the HCVR x-axis intercept (average of ± 1·1 mmHg; ±2·1{\%} of 24 h mean). 4. Despite a significant circadian variation in metabolism (±3·2{\%} of 24 h mean), there were no detectable rhythms in tidal volume, respiratory frequency or ventilation. This small discrepancy between metabolism and ventilation led to a small but significant circadian variation in end-tidal P(CO2) (P(ET,CO2); ±0·6 mmHg; ±1·5{\%} of 24 h mean). 5. The circadian minima of the group-averaged respiratory variables occurred 6-8 h earlier than CBT(min), suggesting that endogenous changes in CBT across the circadian cycle have less of an effect on respiration than equivalent experimentally induced changes in CBT. 6. Throughout these circadian changes, there were no correlations between HCVR parameters (slope or x-axis intercept) and either resting ventilation or resting P(ET,CO2). This suggests that ventilation and P(ET,CO2) are little influenced by central chemosensory respiratory control in awake humans even when at rest under constant environmental and behavioural conditions. 7. The characteristic change in P(ET,CO2) during non-rapid eye movement sleep was shown to be independent of circadian variations in P(ET,CO2), and probably reflects a change from predominantly behavioural to predominantly chemosensory respiratory control. 8. This study has documented the existence and magnitude of circadian variations in respiration and respiratory control in awake humans for the first time under constant behavioural and environmental conditions. These results provide unique insights into respiratory control in awake humans, and highlight the importance of considering the phase of the circadian cycle in studies of respiratory control.",
author = "Spengler, {Christina M.} and Czeisler, {Charles A.} and Steven Shea",
year = "2000",
language = "English (US)",
volume = "526",
pages = "683--694",
journal = "Journal of Physiology",
issn = "0022-3751",
publisher = "Wiley-Blackwell",
number = "3",

}

TY - JOUR

T1 - An endogenous circadian rhythm of respiratory control in humans

AU - Spengler, Christina M.

AU - Czeisler, Charles A.

AU - Shea, Steven

PY - 2000

Y1 - 2000

N2 - 1. Many physiological and behavioural functions have circadian rhythms - endogenous oscillations with a period of approximately 24 h that can occur even in the absence of sleep. We determined whether there is an endogenous circadian rhythm in breathing, metabolism and ventilatory chemosensitivity in humans. 2. Ten healthy, adult males were studied throughout 4 days in a stable laboratory environment. After two initial baseline days (16 h wakefulness plus 8 h sleep) that served to achieve a steady state, subjects were studied under constant behavioural and environmental conditions throughout 41 h of wakefulness. Ventilation, metabolism and the magnitude of the hypercapnic ventilatory response (HCVR) were measured every 2 h. Individuals' data were aligned according to circadian phase (core body temperature minimum; CBT(min)) and averaged. 3. In the group average data, there was a significant and large amplitude circadian variation in HCVR slope (average of ±0·4 1 min -1 mmHg-1; corresponding to ± 12·1% of 24 h mean), and a smaller amplitude rhythm in the HCVR x-axis intercept (average of ± 1·1 mmHg; ±2·1% of 24 h mean). 4. Despite a significant circadian variation in metabolism (±3·2% of 24 h mean), there were no detectable rhythms in tidal volume, respiratory frequency or ventilation. This small discrepancy between metabolism and ventilation led to a small but significant circadian variation in end-tidal P(CO2) (P(ET,CO2); ±0·6 mmHg; ±1·5% of 24 h mean). 5. The circadian minima of the group-averaged respiratory variables occurred 6-8 h earlier than CBT(min), suggesting that endogenous changes in CBT across the circadian cycle have less of an effect on respiration than equivalent experimentally induced changes in CBT. 6. Throughout these circadian changes, there were no correlations between HCVR parameters (slope or x-axis intercept) and either resting ventilation or resting P(ET,CO2). This suggests that ventilation and P(ET,CO2) are little influenced by central chemosensory respiratory control in awake humans even when at rest under constant environmental and behavioural conditions. 7. The characteristic change in P(ET,CO2) during non-rapid eye movement sleep was shown to be independent of circadian variations in P(ET,CO2), and probably reflects a change from predominantly behavioural to predominantly chemosensory respiratory control. 8. This study has documented the existence and magnitude of circadian variations in respiration and respiratory control in awake humans for the first time under constant behavioural and environmental conditions. These results provide unique insights into respiratory control in awake humans, and highlight the importance of considering the phase of the circadian cycle in studies of respiratory control.

AB - 1. Many physiological and behavioural functions have circadian rhythms - endogenous oscillations with a period of approximately 24 h that can occur even in the absence of sleep. We determined whether there is an endogenous circadian rhythm in breathing, metabolism and ventilatory chemosensitivity in humans. 2. Ten healthy, adult males were studied throughout 4 days in a stable laboratory environment. After two initial baseline days (16 h wakefulness plus 8 h sleep) that served to achieve a steady state, subjects were studied under constant behavioural and environmental conditions throughout 41 h of wakefulness. Ventilation, metabolism and the magnitude of the hypercapnic ventilatory response (HCVR) were measured every 2 h. Individuals' data were aligned according to circadian phase (core body temperature minimum; CBT(min)) and averaged. 3. In the group average data, there was a significant and large amplitude circadian variation in HCVR slope (average of ±0·4 1 min -1 mmHg-1; corresponding to ± 12·1% of 24 h mean), and a smaller amplitude rhythm in the HCVR x-axis intercept (average of ± 1·1 mmHg; ±2·1% of 24 h mean). 4. Despite a significant circadian variation in metabolism (±3·2% of 24 h mean), there were no detectable rhythms in tidal volume, respiratory frequency or ventilation. This small discrepancy between metabolism and ventilation led to a small but significant circadian variation in end-tidal P(CO2) (P(ET,CO2); ±0·6 mmHg; ±1·5% of 24 h mean). 5. The circadian minima of the group-averaged respiratory variables occurred 6-8 h earlier than CBT(min), suggesting that endogenous changes in CBT across the circadian cycle have less of an effect on respiration than equivalent experimentally induced changes in CBT. 6. Throughout these circadian changes, there were no correlations between HCVR parameters (slope or x-axis intercept) and either resting ventilation or resting P(ET,CO2). This suggests that ventilation and P(ET,CO2) are little influenced by central chemosensory respiratory control in awake humans even when at rest under constant environmental and behavioural conditions. 7. The characteristic change in P(ET,CO2) during non-rapid eye movement sleep was shown to be independent of circadian variations in P(ET,CO2), and probably reflects a change from predominantly behavioural to predominantly chemosensory respiratory control. 8. This study has documented the existence and magnitude of circadian variations in respiration and respiratory control in awake humans for the first time under constant behavioural and environmental conditions. These results provide unique insights into respiratory control in awake humans, and highlight the importance of considering the phase of the circadian cycle in studies of respiratory control.

UR - http://www.scopus.com/inward/record.url?scp=0033845982&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0033845982&partnerID=8YFLogxK

M3 - Article

C2 - 10922018

AN - SCOPUS:0033845982

VL - 526

SP - 683

EP - 694

JO - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

IS - 3

ER -