Sleep and Body Temperature in "Morning" and "Evening" People

Sleep. 8(4):311-318 1985 Raven Press. New York Sleep and Body Temperature in "Morning" and "Evening" People Jean Foret, *Nathalie Touron, *Odile Benoit, and *Ginette Bouard Laboratoire de Physiologie Neurosensorielle and *U3 INSERM, Paris, France Summary: Three groups of young, normal sleepers were selected as morning types (MTs).1 evening types (ETs), and neither types (NTs) as determined by the Horne and Ostberg questionnaire. Sleep and rectal temperatures were recorded under three conditions: baseline nights (Cond. 1), sleep on the recovery day after 1 night of sleep deprivation (Cond. 2), and sleep on the recovery night after I night and 1 day of sleep deprivation (Cond. 3). During Conds. 1 and 3, when sleep schedules were self-determined, sleep structure and body temperature were similar in MTs, and ETs, and NTs. During Condo 2, however, MTs had poorer sleep, i.e., a smaller percentage of REM sleep and more awakenings, than ETs. This difference can be related to the evolution of temperature during Condo 2; i.e., a temperature increase in the MT and NT and a decrease in the ET. Key Words: Human sleep--morning type-evening type-sleep deprivation-temperature evolution. Classifying individuals as morning types (MTs), evening types (ETs), and neither types (NTs) is based, in addition to everyday observations, on (a) reported sleep schedules (1), (b) subjectively assessed arousal (2,3), and (c) the time of temperature peak (1). Other circadian variables, such as the excretion of catecholamine (norepinephrine) (2), are not significant indicators of type. All studies differentiating MTs from ETs have utilized diurnal measurements. As far as we know, only Webb and Bonnet (4) have studied nocturnal sleep. However, they clearly differentiated only two groups, MTs and ETs, and studied these two groups only in relation to their sleep schedules and the subjective quality of their sleep. Except for the work of Breithaupt et al. (5), few studies have been devoted to the influence of MT/ET typology on sleep when sleep is delayed. The present study investigates the internal sleep structure of MTs and ETs in relation to the temporal evolution of body temperature. METHODS Nineteen healthy young subjects (aged from 20 to 26 years) selected by means of a questionnaire (1) participated as paid volunteers. All subjects were satisfied with both their sleep and diurnal vigilance and had agreed to keep a 2-week sleep log. Subjects were Accepted for publication May 1985. Address correspondence and reprint requests to J. Foret at Laboratoire de Physiologie Neurosensorielle, 15, rue de l'ecole de Medecine, F-75270 Paris, Cedex 06 France. 311

312 J. FORET ET AL. TABLE 1. Bedtimes under the three conditions Condo 1 Cond.2 Cond.3 Typology MT ET NT 2330 h ± 50 min 0730 h ± 12 min 2218 h ± 60 min 2400 h ± 54 min 0748 h ± 24 min 2208 h ± 13 min 2400 h ± 42 min 0739 h ± 24 min 2230 h ± 36 min Condo 1, baseline nights; Condo 2, sleep on the recovery day after 1 night of sleep deprivation; Condo 3, sleep on the recovery night following 1 night and 1 day of sleep deprivation; MT, morning type; ET, evening type; NT, neither type. divided into three classifications according to their questionnaire scores. The classifications and score ranges were as follows: MT, score range 60-68 (5 subjects); ET, score range 23.5-39.5 (4 subjects); NT, score range 48.5-58 (10 subjects). The experimental procedure, as described in Benoit et a1. (6), consisted of two recording sessions 2 weeks apart. In the present paper, sleep data were obtained under three different conditions: baseline sleep (Cond. 1) (average of 3 nights of study), day sleep after 1 night of sleep deprivation (Cond. 2), and night sleep after 1 night and 1 day of sleep deprivation lasting at least 36 h (Cond. 3). Sleep schedules followed for the baseline nights were as close as possible to the subjects' regular habits with each subject determining his or her own bedtime and awakening time. To a large extent, both types of recovery sleep were ad lib. Table 1 shows average bedtimes under the three conditions. A minimum amplitude of delta waves was not used as a criterion for scoring stage 4. Slow wave sleep (SWS) represents stage 3 plus stage 4; sleep onset was defined as the first occurrence of stage 2. Total sleep stages during the entire night and cycle by cycle were computed by means of a package program. Stage 4 and REM sleep latencies were calculated from the onset of stage 2. Total sleep time (TST) corresponded to the time elapsed from sleep onset till awakening. Rectal temperature was continuously monitored and recorded every 15 min during sleep. Oral temperature was measured every 3 h from rising time until bedtime. RESULTS Sleep data Sleep schedules. Table 2 shows bedtimes, awakening times, and duration of sleep for the three groups as outlined by each subject's 2-week sleep log. In contrast to bedtime and awakening time, sleep duration did not differ significantly across groups. TABLE 2. Sleep schedules reported in a 2-wk sleep log Typology Average waking time Average bedtime Average sleep duration MT ET NT Fischer F test 0740 h ± 40 min 0908 h ± 26 min 0805 h ± 36 min F = 7.2 P < 0.006 2329 h ± 77 min 0128 h ± 40 min 2352 h ± 46 min F = 5.9 p<o.q1 481 ± 87 min 444 ± 34 min 485 ± 52 min NS Abbreviations as defined in Table 1. NS, not significant.

SLEEP, TEMPERATURE, AND "MORNINGNESS" 313 TABLE 3. Average sleep characteristics under three conditions First REM SWS duration latency SWSI REM 1 TST (min) (min) REM (%) (min) (min) (min) Condo 1 379.0 ± 91.0 128.8 ± 35.8 18.3 ± 3.9 82.6 ± 23.2 49.7 ± 17.1 11.3 ± 4.5 Cond.2 247.3 ± 49.7 98.8 ± 31.0 14.6 ± 5.5 73.5 ± 40.8 43.7 ± 14.1 13.9 ± 6.4 Cond.3 512.5 ± 48.6 179.7 ± 47.0 18.3 ± 4.1 93.4 ± 37.0 76.5 ± 28.6 10.4 ± 6.8 ANOVA F = 8.3 F = 21.4 F = 4.1 F = 1.6 F = 13.3 F = 1.8 df (2,56) p < 0.0001 p < 0.0001 p < 0.02 NS p < 0.001 NS TST, total sleep time; SWS, slow wave sleep; SWSl, SWS in the first cycle; REM1, length of the first REM period; ANOVA, analysis of variance. Other abbreviations defined in Tables 1 and 2. Comparisons across sleep conditions. The mean differences across sleep conditions, as shown in Table 3, reflect the results of a previous study (6) carried out with a larger population, a population inclusive of the present sample. The differences were significant for the amount of TST, SWS, SWS in the first cycle, and percentage of REM sleep. The values obtained during Condo 2 were smaller than those of Conds. 1 and 3, with the exception of the length of the first REM period. Comparisons across groups within a given sleep condition. During both Conds. 1 and 3, i.e., conditions of night sleep with self-selected schedules, sleep stage duration and sleep organization were not significantly different as a function of MTs and ETs. During Condo 2, however, there were some significant differences across groups (Table 4): MTs had poorer quality sleep (smaller percentage of REM sleep; more wakefulness; and, as a trend, less SWS and a longer latency of the first REM sleep episode) than ETs. NTs generally had intermediate values for the same parameters. Day sleep characteristics. In accordance with other studies, day sleep did not show the characteristics of recovery sleep because its total duration and amounts of SWS and REM sleep were even smaller than those of baseline sleep (Table 3). When the total population was divided into MT, ET, and NT, the average differences were not as apparent in each group. Except for a shorter sleep duration in Condo 2, ETs exhibited no significant differences in percentage of SWS, REM sleep, or wakefulness across all three conditions. For NTs, significant differences across conditions were observed for TST, the first cycle of SWS, TABLE 4. Day sleep characteristics in the three groups MT ET NT ANOVA TST (min) 250.8 ± 26.3 252.5 ± 85.5 250.7 ± 35.5 NS SWS (min) 95.8 ± 24.1 102.2 ± 39.8 98.8 ± 30.5 NS REM (%) 9.6 ± 3.3 18.1 ± 5.7 14.8 ± 4.9 F = 4.3 P < 0.05 Wake (%) 9.3 ± 9.2 0.7 ± 1.0 2.6 ± 2.2 F = 4.3 P < 0.05 Stage 2 latency (min) 5.4 ± 6.1 3.8 ± 2.5 8.6 ± 4.0 NS First REM latency (min) 87.6 ± 59.0 55.5 ± 6.9 73.7 ± 30.9 NS SWSI (min) 48.3 ± loa 36.6 ± 10.9 44.3 ± 15.7 NS REMI (min) 13.4 ± 5.3 13.4 ± 10.8 14.6 ± 5.5 NS Abbreviations as in Tables 1-3.

314 1. FORET ET AL. TABLE 5. Comparisons within groups across conditions Condo 1 Cond.2 Cond.3 ANOVA MT TST (min) 408.4 ± 78.0 236.2 ± 48.0 523.8 ± 72.6 Highly significant SWS amount (min) 105.2 ± 7.2 95.8 ± 24.0 162.2 ± 9.9 F = 26.5 P < 0.001 REM (%) 16.5 ± 5.5 9.6 ± 3.3 16.0 ± 2.4 F = 8.9 p < 0.004 Wake (%) 2.4 ± 2.2 9.3 ± 9.2 2.4 ± 2.0 F = 2.6 P < 0.11 (trend) SWSI (min) 43.4 ± 8.2 48.3 ± 12.7 84.7 ± 19.9 F = 12.3 P < 0.001 NT TST (min) 395.9 ± 28.7 250.7 ± 37.4 503.3 ± 44.0 Highly significant SWS amount (min) 144.5 ± 39.5 98.8 ± 33.4 198.2 ± 52.5 F = 13.7 P < 0.001 SWSI (min) 54.2 ± 21.1 44.3 ± 15.8 84.3 ± 29.9 F = 8.4 P < 0.001 Abbreviations as in Tables 1-3. and total amount of SWS (Table 5). For MTs, in addition to TST and SWS, there were significant differences in the percentage of REM sleep and wakefulness (trend only) (Table 5). These results show a clear relationship between day sleep characteristics and the morningness scale, in that morning people are more disturbed when they have to recover their sleep in the morning. Temperature data A comparison across average temperature curves of the three conditions showed significant differences (ANOVA) from the fourth hour of sleep (Fig. 1). At the end of Condo 2 the temperature was significantly higher than at the end of baseline, Condo 1, whereas at the end of Condo 3 it was significantly lower. Table 6 shows the values of rectal temperature during Conds. 1 and 2 at bedtime, after 6 h of sleep during Condo 1, after 3 h of sleep during Condo 2, and at waking time as a function of the group. While the three groups had an equivalent temperature at sleep onset, ETs had a different temperature evolution: during Condo 1 their temperatures tended to decrease more than that of the two other groups; during Condo 2 their temperatures decreased, while NTs' and MTs' temperatures increased. Figures 2 and 3 display the temperature evolution during Conds. 1 and 2 from sleep onset. DISCUSSION MTs, ETs, and NTs clearly differ in their spontaneous schedules, as other studies have shown (1-3), but their sleep characteristics during baseline nights do not reflect their respective degrees of morningness. When MTs, ETs, and NTs have to sleep during the day, however, some sleep characteristics do differ. Sleep data In the study by Webb and Bonnet (4), when ETs observed the same bedtime as MTs, the subjective quality of the ETs' sleep deteriorated-suggesting that self-determined sleep Sleep. Vol. 8. No.4. 1985

SLEEP, TEMPERATURE, AND "MORNINGNESS" 315 Rectal temperature (O() 36.8 36.7 36.6 36.5 36.4 36.3 36.2 11/,/1 \ l/! It. J! i(rt!... ~..,Il I t f1h1 \ 1 I \\~\i.> j; I I I"".. / i I I I (al NS ** I i "1bi --NS-NS- --*---;;- TcY-****;;;- -- --- l] FIG. 1. Average temperatures as a function of time elapsed since sleep onset on baseline nights, Condo 1 (solid line, squares); on recovery day after 1 night of sleep deprivation, Condo 2 (broken line, stars); and on the recovery night after 1 night and 1 day of sleep deprivation, Condo 3 (dotted line, circles). Differences have been tested between Condo 2 and Condo 1 (Student's t test), Condo 1 and Condo 3 (Student's t test), and across Conds. 1-3 (ANOVA). *p < 0.05, **p < 0.01, ***p < 0.001. NS, not significant. Sleep onset 5 6 Hours after sleep onset 7 TABLE 6. Rectal temperature in Condo 1 and Condo 2 at different times of sleep in the three groups SO 3rd S SR-SO 6th S 6th S-SO SR Cond.1 MT 36.68 ± 0.37 36.52 ± 0.22-0.14 ± 0.33 36.66 ± 0.23 ET 36.75 ± 0.23 36.26 ± 0:24-0.48 ± 0.33 36.34 ± 0.30 NT 36.71 ± 0.36 36.50 ± 0.31-0.21 ± 0.34 36.57 ± 0.35 ANOVA NS F = 2.45 F = 2.84 F = 2.6 df (2,51) (p < 0.10) (p < 0.07) (p < 0.08) Cond.2 MT 36.28 ± 0.42 36. 90 ± 0.30 + 0.70 ± 0.31 36.99 ± 0.33 ET 36.53 ± 0.09 36.41 ± 0.34-0.13 ± 0.48 36.39 ± 0.45 NT 36.75 ± 0.51 36.73 ± 0.22 +0.17 ± 0.43 36.93 ± 0.14 ANOVA NS F = 3.21 F = 3.97 F = 5.82 df (2,14) (p < 0.07) P < 0.04 p < 0.02 Values are means ± SO. SO, sleep onset; S, hour of sleep; SR, rising time. Other abbreviations as in Table 1-3.

316 J. FORET ET AL. FIG. 2. Baseline sleep (Cond. 1). Average temperature curve of the three groups-morning type (solid line, squares); evening type (dotted line, circles); and neither type (broken line, triangles)--relative to the temperature level at sleep onset. Rectal temperature (O() I o _ 0,30 ~ ~ ~\ A \ \\ ~..Lx, " \o.\!y. '. l",,--'t'>.---4 /" 'Y::s:--l:s--~--t!. \./~../\ i \ ~. "....~.'\........ ~.... S.leep onset Hours after sleep onset schedules may be a prerequisite for good sleep. Such schedules are likely to be linked to the diurnal evolution of alertness. Foret et al. (3) found a 2-h difference in the peak of subjective alertness, but no time difference in the temperature peak, for ETs and MTs. The time difference for the peak of alertness between ETs and MTs correlates well with their different sleep schedules. The similarity of sleep patterns across groups during a recovery night after 36 h of sleep deprivation (Cond. 3) suggests that the need for recovery masks interindividual differences, as previously reported in a study of long and short sleepers (7). In contrast, the recovery sleep for the three groups is clearly differentiated when subjects are required to sleep in the morning after 1 night of sleep deprivation (Cond. 2). Under Condo 2, MTs have less REM sleep and more intervening wakefulness than either ETs or NTs. Furthermore, although not statistically significant, the latency of the MTs' first REM sleep episode tends to be longer, which might explain their smaller amount of REM sleep since all three groups (MTs, ETs, and NTs) have the same total sleep duration. It has been demonstrated (8) that a bedtime later than 12 a.m. is a crucial determinant for sleep duration, i.e., the later people go to bed, the shorter their sleep duration. Breithaupt et al. (5) have shown that when MTs and ETs go to bed at 3 a.m. their sleep length differs ETs sleep longer than MTs. We did not find such a difference perhaps because our subjects went to bed an additional 4 h later (-7 a.m.). Thus, such disagreement could be accounted

SLEEP, TEMPERATURE, AND "MORNINGNESS" 317 + 0.5 OJ ' ::J +- +0.3 ~ +0.2 QI c. E ~ +0.1 111 +- :;: 0 c::: -0.1 - O. 2 -U.3 t,,' f:!l. Ai:5. fi eli l-'/ /'.. A t~ ~... fi:...!it... "'J'~.. "fi'" FIG. 3. Sleep recovery day after I night of sleep deprivation (Cond. 2). Average temperature of the three groups-morning type (solid line, squares); evening type (dotted line, circles); and neither type (broken line, triangles)--relative to the temperature at sleep onset. Sleep onset 2 3 Hours after sleep onset for by the stronger "pressure" for sleep that resulted in an equivalent sleep length in MTs, and ETs, although the MTs' sleep was of a poorer quality than that of the ETs., The poor quality of morning sleep in MTs could explain why MTs report more difficulties than ETs in tolerating shift work (9). Temperature data The two main differences across conditions are as follows: (a) The lowest temperature curve occurs during Condo 3. This finding is in agreement with most of the results concerning temperature evolution after sleep deprivation (10-13) but raises the question, as yet still unanswered, of whether such a decrease is related to the special structure of recovery sleep (more SWS and REM sleep at the end of the night and fewer awakenings) or whether it is due to a slow process of homeostatic regulation in response to sleep deprivation. (b) Temperature increases in Condo 2 beginning at the second hour of sleep, as previously reported by Gillberg and Akerstedt (14). In Condo 2, the masking effect of sleep, that lowers temperature after sleep onset, is unable to prevent the circadian tendency toward higher temperature. The three groups do not manifest differences across conditions to the same extent. As a rule, the temperature of ETs is the least affected by the different conditions; thus, during Condo 2 the ETs' temperature decreeases during the first hour and then remains stable. When circadian temperature curves of MTs and ETs are compared, it appears that their bedtimes occur in different places in the circadian temperature curve: prior to and after the temperature trough in ETs and MTs, respectively, as found by Gillberg and Akerstedt (14). Sleep, Vol. 8, No.4. 1985

318 J. FORET ET AL. Sleep and temperature A difference in circadian phase may aiso explain MTs' sleep structure (less REM sleep and more intervening wakefulness), as Breithaupt et al. (5) have shown. But according to Czeisler et al. (15) and Zulley et al. (16), the difference in circadian phase should also have resulted in different sleep durations in MTs and ETs. This may not have occurred because of the pressure of sleep deprivation. That the three groups slept for a similar period of time during the day suggests that awakening time is not completely determined by the temperature but that it could be controlled by another mechanism underlying wakefulness. MTs, ETs, and NTs clearly differ in their spontaneous bedtimes, waking times, and peak vigilance times (3). After a sleep-deprived night, MTs experience more difficulty sleeping in the morning than do ETs. Conversely, ETs are unable to fall asleep when they are made to go to bed at a time that is habitual for MTs. Because temperature curves are similar across the three groups, sleep/wake rhythm shows a larger phase delay relative to temperature rhythm in ETs than in MTs. Only free-running experiments could determine the intrinsic characteristics of the sleep/wake cycle that differentiate MTs from ETs, i. e., longer spontaneous period in ETs and more limited ability to phase advance. Acknowledgment: The authors thank Mr. 1. R. Teilhac for drawing the figures and Mr. 1. Lacombe for assistance in data analysis. This study was partially supported by A.I. CNRS 031640 (0. Benoit). REFERENCES 1. Horne JA, Ostberg O. A self-assessment questionnaire to determine morningness/eveningness. Int J Chronobiol 1976;4:97-110. 2. Akerstedt T, Froberg J. Interindividual differences in circadian patterns of catecholamine excretion, body temperature, performance and subjective arousal. Bioi Psychol 1976;4:277-92. 3. Foret J, Benoit 0, Royant-Parola S. Sleep schedules and peak times of oral temperature and alertness in morning and evening "types." Ergonomics 1982;25:821-7. 4. Webb WB, Bonnet MH. The sleep of "morning" and "evening types." BioI PsychoI1978;7:29-35. 5. Breithaupt H, Hildebrandt G, Dohr 0, Tosch R, Sieber U, Werner M. Tolerance to shift of sleep as related to the individual circadian phase position. Ergonomics 1978;21:767-74. 6. Benoit 0, Foret J, Bouard G. The time course of slow wave sleep and REM-sleep in habitual long and short sleepers: effect of prior wakefulness. Hum Neurobiol 1983;2:91-6. 7. Benoit 0, Foret J, Bouard G, Merle B, Landau J, Marc ME. Habitual sleep length and patterns of recovery sleep after 24 hour and 36 hour sleep deprivation. Electroencephalogr Clin Neurophysiol 1980;50:477-85. 8. Foret J, Lantin G. The sleep of railway engineers. In: Colquhoun WP, ed. Aspects of human efficiency. London: The English Universities Press, 1972:273-82. 9. Hildebrandt G, Stratmann 1. Circadian system response to night work in relation to the individual circadian Rhase position. Int Arch Occup Environ Health 1979;43:73-83. 10. Akerstedt T, Froberg J. Psychophysiological circadian rhythms in women during 72 h of sleep deprivation. Waking Sleeping 1977;1:387-94. II. Aschoff J, Giedke H, Poppel E, Wever R. The influence of sleep interruption and of sleep deprivation on circadian rhythms in human performance. In: Colquhoun WP, ed. Aspects of human efficiency. London: The English Universities Press, 1972:135-50. 12. Froberg J, Karlsson CG, Levi L, Lidberg L. Psychophysiological circadian rhythms during a 72-hour vigil. Forsvarmedicin 1975;11:192-201. 13. Home JA. A review of the biological effects of total sleep deprivation in man. Bioi PsychoI1978;7:55-102. 14. Gillberg M, Akerstedt T. Body temperature and sleep at different times of day. Sleep 1982;5:378-88. 15. Czeisler CA, Weitzman ED, Moore-Ede MC, Zimmerman JC, Knauer RS. Human sleep: its duration and organization depend on its circadian phase. Science 1980;210;1264-7. 16. Zulley J, Wever R, Aschoff J. The dependence of onset and duration of sleep on the circadian rhythm of rectal temperature. Pflugers Arch 1981;391:314--8.