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University of Groningen Body Temperature Predicts the Direction of Internal Desynchronization in Humans Isolated from Time Cues

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University of Groningen Body Temperature Predicts the Direction of Internal Desynchronization in Humans Isolated from Time Cues University of Groningen Body temperature predicts the direction of internal desynchronization in humans isolated from time cues Daan, Serge; Honma, Sato; Honma, Ken-ichi Published in: Journal of Biological Rhythms DOI: 10.1177/0748730413514357 IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2013 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Daan, S., Honma, S., & Honma, K. (2013). Body temperature predicts the direction of internal desynchronization in humans isolated from time cues. Journal of Biological Rhythms, 28(6), 403-411. DOI: 10.1177/0748730413514357 Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 11-02-2018 Body Temperature Predicts the Direction of Internal Desynchronization in Humans Isolated from Time Cues Serge Daan,*,1 Sato Honma, † and Ken-ichi Honma † *Center for Life Sciences, University of Groningen, Groningen, the Netherlands, and †Department of Chronomedicine, Hokkaido University Medical School, Sapporo, Japan Abstract This publication presents a new analysis of experiments that were car- ried out in human subjects in isolation from time cues, under supervision of Jürgen Aschoff and Rütger Wever at the Max Planck Institute for Behavioural Physiology (Erling-Andechs, Germany, 1964-1974). Mean rectal temperatures (t b) were compared between subjects who showed internal desynchronization (ID) and internal synchronization (IS) of the endogenous rhythms of sleep- wakefulness and of body temperature. The results showed that t b was reduced in long ID (circadian sleep-wake cycle length [ WSW] > 27 h) and increased in short ID ( WSW < 22 h) relative to IS. In subjects with both ID and IS sections in the com- plete record, these differences were also found when comparing only the IS sections: Low t b during IS predicts the later occurrence of long ID, and high t b predicts the incidence of short ID. While this association is associated with sex differences in t b, it also occurs within each sex. To the extent that the variation in tb reflects the variation in heat production (metabolic rate), the results are con- sistent with the proposition that the spontaneous frequency of the human sleep- wake oscillator is associated with the metabolic rate, as suggested on the basis of the proportionality of meal frequency and sleep-wake frequency. The finding thus has implications for our views on spontaneous sleep timing. Keywords human sleep-wake rhythm, circadian, internal desynchronization, sex differ- ences, body temperature, metabolic rate Human subjects in prolonged isolation from first observed by Aschoff (1965) shortly after he external time cues often show internal desynchroni- established the endogenous nature of human circa- zation (ID) (Wever, 1979). This is a state in which the dian rhythms (Aschoff and Wever, 1962). Its occur- alternation of sleep and wakefulness is no longer in rence has been confirmed by several other synchrony with the circadian rhythm of body tem- laboratories (Colin et al., 1968; Jouvet et al., 1974; perature; that is, the 2 rhythms simultaneously Weitzman et al., 1979) and was claimed to occur in exhibit different frequencies. The phenomenon was about one third of all subjects living in isolation from This article is dedicated to the memory of Jürgen Aschoff and Rütger Wever, pioneers of human circadian rhythms research, on whose data the work is based. 1. To whom all correspondence should be addressed: Serge Daan, Center for Life Sciences, University of Groningen, Hoofdweg 274, 9765 CN Paterswolde, the Netherlands; e-mail: [email protected]. JOURNAL OF BIOLOGICAL RHYTHMS, Vol. 28 No. 6, December 2013 403-411 DOI: 10.1177/0748730413514357 © 2013 The Author(s) 403 Downloaded from jbr.sagepub.com at University of Groningen on December 19, 2013 404 JOURNAL OF BIOLOGICAL RHYTHMS / December 2013 external time cues (Wever, 1979). In ID, the cycle circadian period, suggesting that bowel movement length of the sleep-wake rhythm is highly variable slowed down in long ID. between individuals. It can be either much shorter Aschoff’s (1993) suggestion of a change in the meta- (16-20 h; “short ID”) or much longer (29-68 h; “long bolic rate was further supported by his analysis of the ID”) than the circadian body temperature rhythm, locomotor activity of subjects in isolation, measured which retains periods virtually always between 24 by motion sensors underneath the floor carpets in the and 26 h (Wever, 1979). It is quite unusual for other isolation unit. These data demonstrated that the total circadian rhythms to display such a large variability amount of activity per wake episode was independent in the period as the sleep-wake rhythm in humans. of the duration of wakefulness ( D) and that activity per As the processes leading to sleep and those leading hour was inversely proportional to D (Aschoff, 1993). to wakefulness still elude our scientific understand- Since this activity can account only for a small part of ing, it would be of great interest to better understand the metabolic rate, Aschoff (1993) suggested that basal physiological correlates of the period of the sleep- metabolism must also have been reduced in long ID. If wake rhythm, here indicated by WSW. this were true, one might hypothesize that the sleep- Aschoff and colleagues (1984, 1986) have specu- wake cycle is controlled by the same process that con- lated that there might be an association of the cycle trols heat production and, while normally entrained to length with the overall rate of metabolism. This approximately 24 h by the circadian pacemaker, can hypothesis was based on patterns of meal timing assume widely different period lengths under the during ID rather than on direct measurements of the influence of the overall energy metabolic rate in condi- metabolic rate. Their analysis yielded intriguing tions of isolation. This would provide new insight into results. The authors reported that subjects retained the nature of the buildup and breakdown of sleep need the habit of taking 3 meals per wake episode when during wakefulness and sleep (“Process S”) (Borbély, the latter became greatly compressed or expanded in 1982; Daan et al., 1984). ID. The intervals between breakfast, lunch, and din- No direct measurements of the human metabolic ner were reduced or increased in proportion to the rate during prolonged isolation from time cues exist duration of wakefulness (Aschoff et al., 1986). Hence, to put this hypothesis to the test. Since body tem- subjects eat breakfast, lunch, and dinner once per WSW perature is a potential correlate of metabolic heat of, say, 18 h in “short” ID and once per WSW of, say, 34 production, we have looked for a possible relation- h in “long” ID (these values are the means reported ship between the mean core body temperature and by Wever [1979]). If meals had the same size in the WSW in ID in existing data. The core body temperature different situations of internal synchronization (IS) has nearly always been recorded in human circadian and ID, this would lead to a substantial increase in experiments. Its analysis, however, usually focused overall food intake in short ID and to a large decrease on the timing of peaks and troughs in the tempera- in long ID. Aschoff et al. (1986) deplored that no pre- ture rhythm and virtually never on the mean values. cise quantitative measurement had been taken of We first analyzed the extensive data published by food intake and body weight in their experiments. Wever (1979) in his monumental book. Encouraged The limited data on body weight demonstrated no by these initial results (Fig. 1), we proceeded to the loss or gain following ID (Aschoff, 1989). The authors original data of Aschoff and Wever and performed an suggested that there may have been differences in the analysis of a sizeable sample of their experiments. metabolic rate associated with meal frequency. This speculation gained support in a study on 8 subjects by Green et al. (1987a, 1987b). These authors did ana- DATABASE lyze meal timing, meal size, and body weight and concluded that in long ID, the caloric intake rate The data that we used are all derived from the decreased on average by 21%, without negatively experiments performed by Professors Jürgen Aschoff affecting body weight. In their sample, short ID did and Rütger Wever in the first isolation facility specifi- not occur. Green et al. (1987b) indeed shared the view cally built for the purpose of studying human circa- that the mechanism responsible for the timing of dian rhythms. In this facility, at the Max Planck sleep and waking is also important for the timing of Institut für Verhaltensphysiologie in Erling-Andechs, meals. In an analysis of the timing of defecation, Germany, experiments were performed from July 6, Aschoff (1994) further showed that the interval from 1964 until December 21, 1989. The facility and the the main evening meal (or from wake-up) until the experiments until 1978 have been described in detail first defecation expanded proportionally with the by Wever (1979).
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