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Dynamics of nap sleep during a 40 hour period
627
Electroencephalography and Clinical Neurophysiology, 1975, 39:627-633 ~ Elsevier Scientific Publishing Company, Amsterdam-Printed in The Netherlands
DYNAMICS
OF NAP
SLEEP DURING
A 40 H O U R
PERIOD x
J . M . MOSES, D . J. HORD, A. LUBIN, L. C. JOHNSON AND P. NAITOH Na~al Health Research Center, San Diego, Calif. 92152 (U.S.A.)
(Accepted for publication: July 11, 1975)
Most hypotheses on the circadian or ultradian cyclicity of sleep stages are based on monophasic nocturnal sleep (i.e., one nocturnal sleep period per 24 h). Napping, or multiphasic sleep, has been given less attention. Webb et al. (1966) and Webb and Agnew (1967) investigated the differential distribution of stage 4 and stage REM (rapid eye movement) during an early morning nap (0900) and during afternoon naps (1230, 1400, and 1600), and reported that stage REM dominated the morning nap, whereas the afternoon nap contained large amounts of stage 4 and very little REM sleep. They explained their findings on the basis of the temporal proximity of the nap to the onset or termination of the regular nighttime sleep period. The early morning nap was quite similar to the last 2 h of nocturnal monophasic sleep, with stage REM dominating, whereas the afternoon nap, particularly the 1600 nap, had stage 4 and stage REM distributions resembling the first portion of regular nighttime sleep. Weitzman et al. (1974) and Carskadon and Dement (1975) reported a stage REM distribution during nap sleep similar to that reported by Webb et al., with the majority of REM sleep occurring between 0600 and 1200. Several studies of nap sleep (Globus 1966; Webb et aL 1966; Kelley et al. 1973; Weitzman et al. 1974; Carskadon and Dement 1975} have This research was supported by the Advanced Research Projects Agency of the Department of Defense under Order No. 1596, Program Codes OD20 and 1D20, and by Department of the Navy, Bureau of Medicine and Surgery, under Task No. M4305.07-3008DAC5. The views and conclusions contained herein are those of the authors and should not be interpreted as necessarily representing the official policies. either expressed or implied, of the Advanced Research Projects Agency, the Department of the Navy, or the U.S. Government.
reported the appearance of REM sleep within 10 min of the first stage 1 episode. Carskadon and Dement refer to this phenomenon as a "sleeponset REM period", or SOREMP. SOREMPs almost never occur in normal nocturnal sleep. Explanations for the SOREMP in naps are inconclusive, but several hypotheses have been advanced. As an extension of Kleitman's (1963) Basic Rest-Activity Cycle (BRAC), it has been suggested (Snyder 1963; Globus 1966; Kripke 1974; Lavie et al. 1974; Weitzman et al. 1974) that the 90-110 min R E M - N R E M cycle does not terminate upon awakening, but continues to operate with the same periodicity throughout the day. Globus (1966) further hypothesized that the occurrence of REM is a function of real time, occurring at the same time from day to day. Thus a SOREMP could appear if a nap happened to coincide with the REM onset "clock". However, the Carskadon and Dement study, in which subjects slept 30 min out of every 90, reported a tendency for REM sleep to recur on alternate 90 min periods, thus suggesting at least a 180 min cycle during multiphasic sleep. The results presented here are part of a larger study concerned with the relative efficiency of napping, exercise or self-regulation of EEG alpha activity for maintaining performance during a 40 h period. Results on performance will be presented elsewhere (Lubin et al. in preparation). This report focuses on the intra-and inter-nap relationships among sleep stages, the distribution of sleep stages during naps, the relation of nap sleep to oral temperature and time of day, and the relative effects of napping and exercise on recovery sleep.
J. M. MOSES et al.
628 TABLE I Experimental schedule. Baseline sleep
Epochs during 40 h*
Recovery sleep
1
2
3
4
5
6
7
8
9
10
1149
1528
185 l
2243
0209
0546
0942
1348
1656
Clock time
2200-0600
0817
Day
Tuesday
Wednesday
Thursday
Post-recovery epochs
2200~0600
11
12
0810
1146
Friday
*Clock times given are average nap start times (N = 20) METHODS
Twenty male Naval Hospital Corps School students, ages 18-22, volunteered for the study. Subjects were randomly assigned to one of two groups: the Nap group (N = 10) or the Exercise group (Ex group, N = 10). The subjects were studied in pairs (1 Nap subject and 1 Ex subject) for 4.5 consecutive days. The first 2 days (Monday and Tuesday) were orientation and training periods; the subjects slept in the laboratory on the first night, but no sleep recordings were made. The second night (Tuesday) was the baseline recording night, on which all subjects retired at 2200 and were awakened at 0600. The 40 h period began at 0600 Wednesday and ended at 2200 Thursday. During the 40 h period, there were 10 epochs of 220 rain each; the first epoch began at about 0800 with 1 h of napping for the Nap group or 1 h of stationary bicycle exercise for the Ex group. The remaining 160 min of each epoch were devoted to various physiological, performance, and mood tests. The rest of the 40 h, a total of 3 h 20 min, was set aside for breaks and meals. The 40 h period was followed by 8 h of recovery sleep (2200 Thursday to 0600 Friday) and two post-recovery epochs (see Table
I). The recording technique for the baseline and recovery nights has been described by Moses et al. (1972). Eye movements were recorded by the common mode rejection technique (Hord 1975). The recording systems for nap sleep and the bicycle apparatus have been described elsewhere (Lubin et al. in preparation). All sleep recordings were scored by J.M, according to the criteria of Rechtschaffen and Kales (1968). Scoring reliability with other
researchers in the laboratory was consistently O/ near 90/o. RESULTS
The sleep recordings of the first 2 subjects run in the Nap group were not used because EOG (electrooculogram) was not recorded. All Nap group analyses are therefore based on an N of 8. The total sleep time (TST) during each nap, stages 2, 4, and REM, and oral temperature (taken approximately midway between .naps) are presented in Fig. 1. Stages 1 and 3 remained fairly constant throughout the 40 h, with a range of 7-13 min and OM min respectively.
~
3Z7
.'/1/"
3Z$ 3Z3 rorAt SL~EP rIME 60
IS STAGE 2
8
~
~' STA~E
4
24.
8.
o
~ STAGE REM
24 16
CLOCK
0s17
1149
ls28
18.~11 2 2 4 , 3 0209
0546
0~b42 1 3 & 8
1656
c4110
1146
TL~
Fig. 1. Distribution of sleep, sleep stages, and oral temperature during naps (N=8).
629
NAP SLEEP DYNAMICS T A B L E II Sleep measures for baseline night and for the 40 h period (N=8). Measure
Baseline
Naps 1 10
Total bed time (min) Percent total sleep time* Percent wake time* Percent stage 1"* Percent stage 2 Percent stage 3 Percent stage 4 Percent stage R E M
480 94.2 4.0 5.4 51.4 7.7 11.4 24.0
600 61.0"** 38.1 *** 19.9"** 39.1 *** 7.4 16.8"** 16.8"**
* Percent of total bed time. ** All sleep stages are expressed in percent of TST. *** Significant difference from baseline at the 0.05 level or better.
Sleep measures for the baseline night and for the 40 h period are given in Table II. TST during the 40 h period averaged 366 min (_+95) (or 294 min of sleep if stage 1 is excluded). The maximum possible TST was 600 min. TST, and stages 2 and REM (in percent of TST) were all significantly lower when summed over all 10 naps than on the baseline night 1. Percent wake, percent stage 1, and percent stage 4 were significantly higher during naps than on the baseline night. The total number of minutes of slow-wave sleep (SWS -- stage 3 and stage 4) during naps was almost identical to that obtained on the baseline night (85 and 86 min, respectively). Analysis of the latencies and sequences of sleep stages made it clear that sleep during a nap does not correspond to the first hour of normal nocturnal bedtime. During baseline sleep, the average REM latency (time from the first stage 1 onset to the onset of the first REM episode) was 68 min, with a range of 48-105 min. For each subject, at least 2 of the 10 naps contained a REM episode. Altogether, REM occurred in 34 of the 80 naps. Twenty-one of the 34 REM episodes were SOREMPs, as defined by Carskadon and Dement (1975) (i.e., appearing within 10 min of stage 1 onset). Eleven of the 21 SOREMPs occurred without prior stage 2. SOREMPs had no clear-cut relation to time of day, although Significance in this paper m e a n s 0.05 level or better, two-tailed test, unless otherwise noted. All t tests were checked by the analogous rank-order Wilcoxon test.
the amount of REM was greatest between the hours 0200-1000. Twenty naps contained both SWS and REM ; in only 2 naps was the REM period preceded by SWS.
The R E M cycle during naps We compressed the sleep time in the 10 naps (excluding all wake time between naps and within a nap), starting with the last REM onset on the baseline night and ending with the first REM onset on the recovery night; this was viewed as one continuous sleep session. We then computed the REM cycle period (the sleep time between two successive REM onset) for each subject. The average REM cycle period in naps was 103 min (_+21), and was not significantly different from the baseline night REM cycle period of 97 min (+ 12). Circadian o'cles and oral temperature Fig. 1 shows that oral temperature followed a near-sinusoidal 24 h cycle throughout the 40 h period. For each subject we assumed that his oral temperature was the best indicator of the circadian cycle. To assess the circadian effect within each subject, oral temperature measures preceding a nap were cross-correlated (Kendall and Stuart 1966) with sleep measures across the 10 naps. Table III presents the correlations for each subject as well as the group means. Since the 8 correlations for each pair of variables were independent, a t test was used to test the group average for significant deviation from zero (the Fisher z transformation was unnecessary). The temperature-circadian effect was significant for TST and minutes of stage REM, with total sleep and REM sleep being greatest when temperature was lowest. The correlations of REM latency and sleep latency (TB2, time from "lights out" to stage 2 onset) with oral temperature were not significant. Note that oral temperature readings preceded the nap by about 90 min. When temperature following the nap was used, the correlations fell to near-zero. From the circadian hypothesis, sleep in nap 5 (beginning at about 2240, which is close to the subject's habitual retiring time) should be similar to sleep in the first hour of the baseline night. The mean differences in sleep stage per-
630
J.M. MOSESet al.
TABLE III Within-subject correlations of oral temperature with nap sleep measures. Subject
TST
Stage 2
Stage 4
Stage REM
03N 04N 05N 06N 07N 08N 09N 10N
+0.03 -0.37 -0.80 -0.47 -0.33 -0.81 +0.21 -0.66
+0.43 -0.13 -0.45 -0.17 +0.34 -0.75 +0.28 -0.41
-0.24 -0.46 -0.73 +0.16 +0.49 -0.54 -0.23 -0.28
-0.33 -0.53 --0.39 --0.63 - 0.60 - 0.43 q- 0.27 - 0.64
S.D.
-0.40* 0.369
-0.11 0,424
-0.23 0.389
-0.41' 0.299
* Significant deviation from zero at the .02 level or better.
cents and latencies between nap 5 and baseline hour 1 were tested for significance from zero with a t test (N=8). There were no significant differences in the amounts or latencies of the various sleep stages. In addition, nap 5 was the only nap containing no stage R E M ; similary, the first baseline hour contained less than 1 stage REM. The feedback effect If R E M sleep duration is governed by a simple negative feedback mechanism, which the results of the Carskadon and Dement (1975) study suggest, then a nap with a long REM duration will be followed by a nap with little or no REM. One way of testing for such negative feedback effects is by auto-correlation (Kendall and Stuart 1966). Within each subject, the amount (in minutes) of R E M sleep on nap 1 was paired with the amount of R E M on nap 2, the amount of REM sleep on nap 2 was paired with the amount of R E M on nap 3, and so on. The resulting correlation across the 9 pairs of values (lag-one auto-correlation) would be negative if the sleep stage tends to alternate. In Table IV are the average lag-one autocorrelations for wake (W) and for stages 2, 4, and R E M in the diagonal cells of the matrix. For comparison, the lag-one auto-correlations for the 8 successive hours of baseline sleep are also given. Negative feedback for stage REM was
present during baseline night sleep, but in nap sleep, none of the sleep stages consistently predicted themselves from one nap to the next. W time had the only significant auto-correlation during naps, and this relationship was positive instead of negative. This indicated that naps with long W times were followed by naps with long W times, and naps with short W times were followed by naps with short W times. This is consistent with a smooth circadian cycle, rather than short-term negative feedback. If sleep stages are not self-regulating, then perhaps the duration of one sleep stage influences the duration of another sleep stage on the next nap (i.e., cross-feedback). This hypothesis was tested by the lag-one cross-correlation between two different sleep stages. For example, within each subject, the amount of REM on nap 1 was paired with the amount of stage 4 on nap 2, the amount of REM nap 2 was paired with the amount of stage 4 on nap 3, and so on. The result is a lag-one cross-correlation, with stage REM (R~) leading stage 4 (42). In Table IV, this cross-correlation between R 1 and 42, averaged over all 8 subjects, was 0.47, significantly greater than zero. When stage 4 leads stage R E M (41 with R2), the lag-one cross-correlation was 0.39, also significant. These results show that large amounts of stage REM lead to large amounts of stage 4 on the next nap, and vice versa. The corresponding cross-correlations for TABLE IV Lag-one auto-correlations (diagonal values) and cross-correlations (off-diagonal values) across naps and across hours of baseline sleep. Measures with subscript 1 lead measures with subscript 2 by 220 rain.
Wl +0.31"
21 -0.12
41 -0.18
R~ -0.30*
w~ (+0.08) (+0.08) (+0.03) (-o.12) 22
-0.31" (-0.22)*
+0.16 (-0.11)
+0.08 (+0.01)
+0.15 (+0.25)*
42
-0.11 (+0.36)
-0.25* (-0.47)*
-0.04 (+0.09)
+0.47* (+0.10)
R2
-0.17 (-0.05)
+0.11 (+0.43)*
+0.39* -0.10 (+0.007)(-0.34)*
Note: Values in ( ) are for baseline night hours. * Significant at 0.05 or better.
NAP SLEEP DYNAMICS
the hours of baseline nocturnal sleep did not show this reciprocal positive relation for stage REM and stage 4. The significant cross-correlations for stages 2 and REM on the baseline night suggest such a cross-feedback effect, but no simple hypothesis emerges for the remaining significant cross-correlations. Naps, exercise and recovery sleep
For the Nap group, there was only one significant difference between baseline and allnight recovery sleep. Sleep latency (TB2) increased from 22 rain on the baseline night to 37 min on the recovery night. For the Ex group, those subjects who pedaled a bicycle instead of napping, there was a significant increase in stage 4 on recovery (from 52 to 103 min), and significant decreases from baseline in stage 1 (from 36 to 6 min) and TB2 (from 34 to 9 min). Between-group analysis of the recovery night showed that the Ex group had significantly less W time, stage 1, and stage REM than the Nap group, and had shorther latencies to stages 2, 4, and REM. The Ex group also had significantly more TST and stage 4. Post-recovery sleep naps
There were no significant differences between naps 1 (Wednesday, 0817) and 11 (Friday, 0810) both of which immediately followed 8 h of uninterrupted sleep. The sleep measures from nap 12 were not used because of a possible end-of-experiment effect. DISCUSSION
As Weitzman et al. (1974) aptly stated, naps are "clearly not miniatures of the normal 8-hr sleep pattern". Our data also show that naps are not replicas of the first hour of the 8 h pattern, except when a nap coincides with the habitual retiring time. Since REM is often found in a 1 h nap and frequently follows stage 1 onset, the organization of sleep within a nap must differ from that in normal monophasic nocturnal sleep. While the usual stage 2, 3, 4 sequence was preserved in nap sleep, only 2 of the 20 naps containing both SWS and stage REM showed the usual temporal sequence of stage REM following SWS. In the Weitzman et al. (1974) study of 560 1 h naps at 3 h intervals, there was a
631 sequence reversal of SWS and REM in about half of the 89 naps in which these stages occurred together. The circadian rhythmicity of body temperature is well documented, and we found, as did Weitzman et al. (1974), that TST was entrained to the temperature cycle, with sleep efficiency (TST/Total Bed Time) being maximal when temperature was lowest. While temperature is closely related to the ability to fall asleep and remain asleep, several other factors appear to influence the sleep stages. The relationships of the sleep stages from one nap to the next differed from their hour-to-hour relationships on the baseline night. The reciprocal positive relation between stage 4 and stage REM appears to be unique to naps. In monophasic nocturnal sleep, stage REM regulated itself from one hour to the next, and was independent of the amount of stage 4 in a preceding or subsequent hour. In contrast to the REM alternation reported by Carskadon and Dement (1975), in our study, REM did not predict itself from one nap to the next. The waking period between naps apparently facilitated the stage 4-stage REM feedback since such feedback did not exist in continuous sleep. On the other hand, the waking period interfered with the self-regulation of stage REM, since the negative feedback observed in nocturnal continuous sleep did not occur in naps. Ephron and Carrington (1966) and Berger (1969) have hypothesized that the function of REM sleep is to increase cortical and oculomotor activity during sleep. The assumption is that during sleep, periodic activation of these systems to waking levels is necessary for efficient functioning during the subsequent waking state. Freemon (1972, p. 152) stated the REM activation hypothesis as "each rem period could be replaced by a period of wakefulness". This hypothesis is clearly refuted by the fact that waking periods between naps do not inhibit or substitute for REM sleep. As noted earlier, it has been suggested that the 90-110 min REM cycle in sleep continues to operate with the same periodicity throughout the waking state (a sleep-independent clock): 90-110 min cycles have been found in arousal level, gastric motility, and some hormone secretions. Although a thorough analysis and
632
J.M. MOSESet al.
discussion of the ultradian REM cycle clock are Total sleep time and the amount of stage not intended for this report, the results of our REM during the naps were negatively related to REM cycle analysis indicate that the clock the circadian-temperature cycle. Stage REM governing the REM cycle is sleep-dependent-- frequently appeared within 10 min of stage 1 it stops upon awakening and resumes at the next onset and the normal sequence of stages REM sleep onset. This suggests that the 90-110 rain and 4 were altered, demonstrating that the cycles found in the awake subject are not ex- organization of sleep within a nap is quite differpressions of the 90-110 min REM cycle found ent from that in monophasic nocturnal sleep. during sleep. Auto-correlation and cross-correlation analyses Although TST during the 10 naps was lower showed that the relation of sleep stages from than baseline, the relatively small amount of hour to hour in normal continuous baseline sleep sleep loss incurred by napping was not sufficient was altered in nap-to-nap comparison. The to produce the changes in recovery sleep timing of REM onset may be controlled by a usually associated with sleep loss. But the reco- sleep-dependent ultradian clock; the clock may very night for the Ex group looked much like stop upon awakening and resume at the next sleep typical recovery sleep following sleep loss of 1-2 onset. Naps had recuperative value in terms of nights. Shorter sleep latencies, reduced W time, maintaining the normal amounts of sleep stages and greatly augmented stage 4 were present. on the recovery night; recovery sleep for the Because no such differences were found be- exercise group showed typical sleep-loss effects. tween baseline and recovery for the Nap group, naps presumably have some recuperative value, RESUME at least in terms of preserving the normal amounts DYNAMIQUE DU SOMMEIL DE SIESTE AU COURS and distribution of sleep stages during recovery D'UNE PERIODE DE 4 0 HEURES sleep. The length of time the subject is on the nap sleep regime, however, seems to be impor- Apr~s une nuit de contr61e, le sommeil de 8 tant in determining sleep patterns on the recovery sujets mfiles adultes r6parti en siestes d'une heure, night. In the Weitzman et al. (1974) and Carska- 6galement espac6e au cours d'une p6riode de don and Dement (1975) studies, subjects were 40 h, est explor6. 10 sujets additionnels ont 6t6 maintained on the nap sleep schedule much privds de sommeil pendant 40 h avec des p6riodes longer (10 and 5 days repectively) than the 40 h d'une heure d'exercice donn6es fi la place des of the present study, and both of those studies siestes. Une nuit de r6cup6ration suit la p6riode reported sleep-deprivation effects on the reco- de 40 h pour les deux groupes. very nights. Le temps de sommeil total et la quantit6 de Sleep during naps cannot be accounted for sommeil paradoxal au cours des siestes est en exclusively within the framework of what we liaison n6gative avec le cycle circadien de la temknow about monophasic nocturnal sleep. The p6rature. Le sommeil paradoxal apparait fr6results of this study show that no single factor quemment au cours des 10 premi6res rain de Fendetermines the type of sleep that will occur in a dormissement en stade I, et la s6quence normale, given nap, and the hypotheses put forth to de sommeil paradoxal et de stade IV est alt6r6e, explain the dynamics of nap sleep overlap montrant que l'organisation du sommeil considerably. l'int6rieur d'une sieste est tout fi fait diff6rente de ce qu'elle est dans le sommeil nocturne SUMMARY monophasique. Des analyses d'auto-corr61ation et de cross-corr61ation montrent que la relation Following 1 baseline night, the sleep of 8 adult des stades du sommeil d'heure en heure au cours males in equally spaced 1 h naps during a 40 h du sommeil normal continu lors de la nuit de period was examined. Ten additional subjects contr61e est alt6r6e dans les s6quences comparawere sleep-deprived for 40 h with 1 h periods of tives sieste-~t-sieste. On peut penser que la exercise given in place of naps. One recovery survenue temporelle de l'endormissement en night followed the 40 h period for both groups. sommeil paradoxal est contr616e par une horloge
NAP SLEEP DYNAMICS
ultradienne d~pendant du sommeil ; cette horloge peut s'arr&er lors de l'6veil et reprendre au prochain endormissement. Les siestes ont une valeur r6paratoire en ce sens qu'elles maintiennent les quantit6s normales de stades de sommeil au cours de la nuit de r6cup6ration" le sommeil, lors de la nuit de r6cup6ration dans le groupe qui a subi les exercices montre les effets typiques de manque de sommeil. REFERENCES BERGER, R. J. Oculomotor control: a possible function of REM sleep. Psychol. Rev., 1969, 76: 144-164. CARSKADON,M. A. and DEMENT, W. C. Sleep studies on a 90-minute day. Electroenceph. clin. Neurophysiol.. 1975, 39: 145-155. EPHRON, H. S. and CARRINGTON,P. Rapid eye movement sleep and cortical homeostasis. Psychol. Rer.. 1966, 73: 500-526. FREEMON, F. R. Sleep research. Thomas, Springfield, Ill.. 1972, 205 p. GLOBUS, G. G. Rapid eye movement cycle in real time. Arch 9en. Psychiat., 1966, 15: 654-659. HORD, D. Common mode rejection techniques in conjugate eye movement recording during sleep. Psychophysioloqy, 1975, 12: 354-355. KELLEY, J., LAUGHLIN, E., CARPENTER, S., SIMMONS, J.. SIDORIC, K. and LENTZ, R. A study of ninety-minute sleep cycles. Stanford Review, 1973, 3: 1-5. KENDALL, M. G. and STUART, A. The advanced theory of statistics, VoL HI. Griffin. London, 1966. KLEITMAN, N. Sleep and wakefulness. University of Chicago
633 Press, Chicago, II1., 1%3, 552 p. KRIPKE, D. F. Ultradian rhythms in sleep and wakefulness. In E. D. WEITZMAN (Ed.), Advances in sleep research, Vol. 1. Spectrum Publications, a subsidiary of Wiley, New York, 1974: 305-325. LAVlE, P., LORD, J. W. and FRANK, R. A. Basic rest-activity cycle in the perception of the spiral after-effect: a sensitive detector of a basic biological rhythm. Behar. Biol.. 1974, I1~ 373--379. LUBIN, A., HORD, D. J., TRACY, M. L. and. JOHNSON, L. C. Effects of exercise bedrest and napping on performance decrement during 40 hours. Submitted to Psychophysiology. MOSES, J., LUBIN, A., NAITOH, P. and JOHNSON, L. C. Reliability of sleep measures. Psychophysioloyy, 1972, 9: 78 82. RECHTSCHAFFEN, A. and KALES, A. (Eds.). A manual o/ standardized terminology, techniques and scoring system jor sleep stages of human sut~jects. Public Health Service, U.S. Government Printing Office, Washington, D.C., 1968. SNYDER, F. The new biology of dreaming. Arch. #en. Psychiat., 1963, 8." 381 391. WEBB, W. B. and AGNEW JR., H. W. Sleep cycling within twenty-four hour periods. J. exp. Physiol., 1967, 74: 158-160. WEBB, W. B., AGNEW JR., H, W. and STERNTr~AL, H. Sleep during the early morning. Psychonom. Sci., 1966, 6: 277 278. WEITZMAN,E. D., NOGEIRE,C., PERLOW,M., FUKUSHIMA,D., SASSIN, J., MCGREGOR, P., GALLAGHER,T. F. and HELLMAN, L. Effects of a prolonged 3-hour sleel~wake cycle on sleep stages, plasma cortisol, growth hormone and body temperature in man. J. clin. Endocr., 1974, 38: 1018 1030.
Electroencephalography and Clinical Neurophysiology, 1975, 39:627-633 ~ Elsevier Scientific Publishing Company, Amsterdam-Printed in The Netherlands
DYNAMICS
OF NAP
SLEEP DURING
A 40 H O U R
PERIOD x
J . M . MOSES, D . J. HORD, A. LUBIN, L. C. JOHNSON AND P. NAITOH Na~al Health Research Center, San Diego, Calif. 92152 (U.S.A.)
(Accepted for publication: July 11, 1975)
Most hypotheses on the circadian or ultradian cyclicity of sleep stages are based on monophasic nocturnal sleep (i.e., one nocturnal sleep period per 24 h). Napping, or multiphasic sleep, has been given less attention. Webb et al. (1966) and Webb and Agnew (1967) investigated the differential distribution of stage 4 and stage REM (rapid eye movement) during an early morning nap (0900) and during afternoon naps (1230, 1400, and 1600), and reported that stage REM dominated the morning nap, whereas the afternoon nap contained large amounts of stage 4 and very little REM sleep. They explained their findings on the basis of the temporal proximity of the nap to the onset or termination of the regular nighttime sleep period. The early morning nap was quite similar to the last 2 h of nocturnal monophasic sleep, with stage REM dominating, whereas the afternoon nap, particularly the 1600 nap, had stage 4 and stage REM distributions resembling the first portion of regular nighttime sleep. Weitzman et al. (1974) and Carskadon and Dement (1975) reported a stage REM distribution during nap sleep similar to that reported by Webb et al., with the majority of REM sleep occurring between 0600 and 1200. Several studies of nap sleep (Globus 1966; Webb et aL 1966; Kelley et al. 1973; Weitzman et al. 1974; Carskadon and Dement 1975} have This research was supported by the Advanced Research Projects Agency of the Department of Defense under Order No. 1596, Program Codes OD20 and 1D20, and by Department of the Navy, Bureau of Medicine and Surgery, under Task No. M4305.07-3008DAC5. The views and conclusions contained herein are those of the authors and should not be interpreted as necessarily representing the official policies. either expressed or implied, of the Advanced Research Projects Agency, the Department of the Navy, or the U.S. Government.
reported the appearance of REM sleep within 10 min of the first stage 1 episode. Carskadon and Dement refer to this phenomenon as a "sleeponset REM period", or SOREMP. SOREMPs almost never occur in normal nocturnal sleep. Explanations for the SOREMP in naps are inconclusive, but several hypotheses have been advanced. As an extension of Kleitman's (1963) Basic Rest-Activity Cycle (BRAC), it has been suggested (Snyder 1963; Globus 1966; Kripke 1974; Lavie et al. 1974; Weitzman et al. 1974) that the 90-110 min R E M - N R E M cycle does not terminate upon awakening, but continues to operate with the same periodicity throughout the day. Globus (1966) further hypothesized that the occurrence of REM is a function of real time, occurring at the same time from day to day. Thus a SOREMP could appear if a nap happened to coincide with the REM onset "clock". However, the Carskadon and Dement study, in which subjects slept 30 min out of every 90, reported a tendency for REM sleep to recur on alternate 90 min periods, thus suggesting at least a 180 min cycle during multiphasic sleep. The results presented here are part of a larger study concerned with the relative efficiency of napping, exercise or self-regulation of EEG alpha activity for maintaining performance during a 40 h period. Results on performance will be presented elsewhere (Lubin et al. in preparation). This report focuses on the intra-and inter-nap relationships among sleep stages, the distribution of sleep stages during naps, the relation of nap sleep to oral temperature and time of day, and the relative effects of napping and exercise on recovery sleep.
J. M. MOSES et al.
628 TABLE I Experimental schedule. Baseline sleep
Epochs during 40 h*
Recovery sleep
1
2
3
4
5
6
7
8
9
10
1149
1528
185 l
2243
0209
0546
0942
1348
1656
Clock time
2200-0600
0817
Day
Tuesday
Wednesday
Thursday
Post-recovery epochs
2200~0600
11
12
0810
1146
Friday
*Clock times given are average nap start times (N = 20) METHODS
Twenty male Naval Hospital Corps School students, ages 18-22, volunteered for the study. Subjects were randomly assigned to one of two groups: the Nap group (N = 10) or the Exercise group (Ex group, N = 10). The subjects were studied in pairs (1 Nap subject and 1 Ex subject) for 4.5 consecutive days. The first 2 days (Monday and Tuesday) were orientation and training periods; the subjects slept in the laboratory on the first night, but no sleep recordings were made. The second night (Tuesday) was the baseline recording night, on which all subjects retired at 2200 and were awakened at 0600. The 40 h period began at 0600 Wednesday and ended at 2200 Thursday. During the 40 h period, there were 10 epochs of 220 rain each; the first epoch began at about 0800 with 1 h of napping for the Nap group or 1 h of stationary bicycle exercise for the Ex group. The remaining 160 min of each epoch were devoted to various physiological, performance, and mood tests. The rest of the 40 h, a total of 3 h 20 min, was set aside for breaks and meals. The 40 h period was followed by 8 h of recovery sleep (2200 Thursday to 0600 Friday) and two post-recovery epochs (see Table
I). The recording technique for the baseline and recovery nights has been described by Moses et al. (1972). Eye movements were recorded by the common mode rejection technique (Hord 1975). The recording systems for nap sleep and the bicycle apparatus have been described elsewhere (Lubin et al. in preparation). All sleep recordings were scored by J.M, according to the criteria of Rechtschaffen and Kales (1968). Scoring reliability with other
researchers in the laboratory was consistently O/ near 90/o. RESULTS
The sleep recordings of the first 2 subjects run in the Nap group were not used because EOG (electrooculogram) was not recorded. All Nap group analyses are therefore based on an N of 8. The total sleep time (TST) during each nap, stages 2, 4, and REM, and oral temperature (taken approximately midway between .naps) are presented in Fig. 1. Stages 1 and 3 remained fairly constant throughout the 40 h, with a range of 7-13 min and OM min respectively.
~
3Z7
.'/1/"
3Z$ 3Z3 rorAt SL~EP rIME 60
IS STAGE 2
8
~
~' STA~E
4
24.
8.
o
~ STAGE REM
24 16
CLOCK
0s17
1149
ls28
18.~11 2 2 4 , 3 0209
0546
0~b42 1 3 & 8
1656
c4110
1146
TL~
Fig. 1. Distribution of sleep, sleep stages, and oral temperature during naps (N=8).
629
NAP SLEEP DYNAMICS T A B L E II Sleep measures for baseline night and for the 40 h period (N=8). Measure
Baseline
Naps 1 10
Total bed time (min) Percent total sleep time* Percent wake time* Percent stage 1"* Percent stage 2 Percent stage 3 Percent stage 4 Percent stage R E M
480 94.2 4.0 5.4 51.4 7.7 11.4 24.0
600 61.0"** 38.1 *** 19.9"** 39.1 *** 7.4 16.8"** 16.8"**
* Percent of total bed time. ** All sleep stages are expressed in percent of TST. *** Significant difference from baseline at the 0.05 level or better.
Sleep measures for the baseline night and for the 40 h period are given in Table II. TST during the 40 h period averaged 366 min (_+95) (or 294 min of sleep if stage 1 is excluded). The maximum possible TST was 600 min. TST, and stages 2 and REM (in percent of TST) were all significantly lower when summed over all 10 naps than on the baseline night 1. Percent wake, percent stage 1, and percent stage 4 were significantly higher during naps than on the baseline night. The total number of minutes of slow-wave sleep (SWS -- stage 3 and stage 4) during naps was almost identical to that obtained on the baseline night (85 and 86 min, respectively). Analysis of the latencies and sequences of sleep stages made it clear that sleep during a nap does not correspond to the first hour of normal nocturnal bedtime. During baseline sleep, the average REM latency (time from the first stage 1 onset to the onset of the first REM episode) was 68 min, with a range of 48-105 min. For each subject, at least 2 of the 10 naps contained a REM episode. Altogether, REM occurred in 34 of the 80 naps. Twenty-one of the 34 REM episodes were SOREMPs, as defined by Carskadon and Dement (1975) (i.e., appearing within 10 min of stage 1 onset). Eleven of the 21 SOREMPs occurred without prior stage 2. SOREMPs had no clear-cut relation to time of day, although Significance in this paper m e a n s 0.05 level or better, two-tailed test, unless otherwise noted. All t tests were checked by the analogous rank-order Wilcoxon test.
the amount of REM was greatest between the hours 0200-1000. Twenty naps contained both SWS and REM ; in only 2 naps was the REM period preceded by SWS.
The R E M cycle during naps We compressed the sleep time in the 10 naps (excluding all wake time between naps and within a nap), starting with the last REM onset on the baseline night and ending with the first REM onset on the recovery night; this was viewed as one continuous sleep session. We then computed the REM cycle period (the sleep time between two successive REM onset) for each subject. The average REM cycle period in naps was 103 min (_+21), and was not significantly different from the baseline night REM cycle period of 97 min (+ 12). Circadian o'cles and oral temperature Fig. 1 shows that oral temperature followed a near-sinusoidal 24 h cycle throughout the 40 h period. For each subject we assumed that his oral temperature was the best indicator of the circadian cycle. To assess the circadian effect within each subject, oral temperature measures preceding a nap were cross-correlated (Kendall and Stuart 1966) with sleep measures across the 10 naps. Table III presents the correlations for each subject as well as the group means. Since the 8 correlations for each pair of variables were independent, a t test was used to test the group average for significant deviation from zero (the Fisher z transformation was unnecessary). The temperature-circadian effect was significant for TST and minutes of stage REM, with total sleep and REM sleep being greatest when temperature was lowest. The correlations of REM latency and sleep latency (TB2, time from "lights out" to stage 2 onset) with oral temperature were not significant. Note that oral temperature readings preceded the nap by about 90 min. When temperature following the nap was used, the correlations fell to near-zero. From the circadian hypothesis, sleep in nap 5 (beginning at about 2240, which is close to the subject's habitual retiring time) should be similar to sleep in the first hour of the baseline night. The mean differences in sleep stage per-
630
J.M. MOSESet al.
TABLE III Within-subject correlations of oral temperature with nap sleep measures. Subject
TST
Stage 2
Stage 4
Stage REM
03N 04N 05N 06N 07N 08N 09N 10N
+0.03 -0.37 -0.80 -0.47 -0.33 -0.81 +0.21 -0.66
+0.43 -0.13 -0.45 -0.17 +0.34 -0.75 +0.28 -0.41
-0.24 -0.46 -0.73 +0.16 +0.49 -0.54 -0.23 -0.28
-0.33 -0.53 --0.39 --0.63 - 0.60 - 0.43 q- 0.27 - 0.64
S.D.
-0.40* 0.369
-0.11 0,424
-0.23 0.389
-0.41' 0.299
* Significant deviation from zero at the .02 level or better.
cents and latencies between nap 5 and baseline hour 1 were tested for significance from zero with a t test (N=8). There were no significant differences in the amounts or latencies of the various sleep stages. In addition, nap 5 was the only nap containing no stage R E M ; similary, the first baseline hour contained less than 1 stage REM. The feedback effect If R E M sleep duration is governed by a simple negative feedback mechanism, which the results of the Carskadon and Dement (1975) study suggest, then a nap with a long REM duration will be followed by a nap with little or no REM. One way of testing for such negative feedback effects is by auto-correlation (Kendall and Stuart 1966). Within each subject, the amount (in minutes) of R E M sleep on nap 1 was paired with the amount of R E M on nap 2, the amount of REM sleep on nap 2 was paired with the amount of R E M on nap 3, and so on. The resulting correlation across the 9 pairs of values (lag-one auto-correlation) would be negative if the sleep stage tends to alternate. In Table IV are the average lag-one autocorrelations for wake (W) and for stages 2, 4, and R E M in the diagonal cells of the matrix. For comparison, the lag-one auto-correlations for the 8 successive hours of baseline sleep are also given. Negative feedback for stage REM was
present during baseline night sleep, but in nap sleep, none of the sleep stages consistently predicted themselves from one nap to the next. W time had the only significant auto-correlation during naps, and this relationship was positive instead of negative. This indicated that naps with long W times were followed by naps with long W times, and naps with short W times were followed by naps with short W times. This is consistent with a smooth circadian cycle, rather than short-term negative feedback. If sleep stages are not self-regulating, then perhaps the duration of one sleep stage influences the duration of another sleep stage on the next nap (i.e., cross-feedback). This hypothesis was tested by the lag-one cross-correlation between two different sleep stages. For example, within each subject, the amount of REM on nap 1 was paired with the amount of stage 4 on nap 2, the amount of REM nap 2 was paired with the amount of stage 4 on nap 3, and so on. The result is a lag-one cross-correlation, with stage REM (R~) leading stage 4 (42). In Table IV, this cross-correlation between R 1 and 42, averaged over all 8 subjects, was 0.47, significantly greater than zero. When stage 4 leads stage R E M (41 with R2), the lag-one cross-correlation was 0.39, also significant. These results show that large amounts of stage REM lead to large amounts of stage 4 on the next nap, and vice versa. The corresponding cross-correlations for TABLE IV Lag-one auto-correlations (diagonal values) and cross-correlations (off-diagonal values) across naps and across hours of baseline sleep. Measures with subscript 1 lead measures with subscript 2 by 220 rain.
Wl +0.31"
21 -0.12
41 -0.18
R~ -0.30*
w~ (+0.08) (+0.08) (+0.03) (-o.12) 22
-0.31" (-0.22)*
+0.16 (-0.11)
+0.08 (+0.01)
+0.15 (+0.25)*
42
-0.11 (+0.36)
-0.25* (-0.47)*
-0.04 (+0.09)
+0.47* (+0.10)
R2
-0.17 (-0.05)
+0.11 (+0.43)*
+0.39* -0.10 (+0.007)(-0.34)*
Note: Values in ( ) are for baseline night hours. * Significant at 0.05 or better.
NAP SLEEP DYNAMICS
the hours of baseline nocturnal sleep did not show this reciprocal positive relation for stage REM and stage 4. The significant cross-correlations for stages 2 and REM on the baseline night suggest such a cross-feedback effect, but no simple hypothesis emerges for the remaining significant cross-correlations. Naps, exercise and recovery sleep
For the Nap group, there was only one significant difference between baseline and allnight recovery sleep. Sleep latency (TB2) increased from 22 rain on the baseline night to 37 min on the recovery night. For the Ex group, those subjects who pedaled a bicycle instead of napping, there was a significant increase in stage 4 on recovery (from 52 to 103 min), and significant decreases from baseline in stage 1 (from 36 to 6 min) and TB2 (from 34 to 9 min). Between-group analysis of the recovery night showed that the Ex group had significantly less W time, stage 1, and stage REM than the Nap group, and had shorther latencies to stages 2, 4, and REM. The Ex group also had significantly more TST and stage 4. Post-recovery sleep naps
There were no significant differences between naps 1 (Wednesday, 0817) and 11 (Friday, 0810) both of which immediately followed 8 h of uninterrupted sleep. The sleep measures from nap 12 were not used because of a possible end-of-experiment effect. DISCUSSION
As Weitzman et al. (1974) aptly stated, naps are "clearly not miniatures of the normal 8-hr sleep pattern". Our data also show that naps are not replicas of the first hour of the 8 h pattern, except when a nap coincides with the habitual retiring time. Since REM is often found in a 1 h nap and frequently follows stage 1 onset, the organization of sleep within a nap must differ from that in normal monophasic nocturnal sleep. While the usual stage 2, 3, 4 sequence was preserved in nap sleep, only 2 of the 20 naps containing both SWS and stage REM showed the usual temporal sequence of stage REM following SWS. In the Weitzman et al. (1974) study of 560 1 h naps at 3 h intervals, there was a
631 sequence reversal of SWS and REM in about half of the 89 naps in which these stages occurred together. The circadian rhythmicity of body temperature is well documented, and we found, as did Weitzman et al. (1974), that TST was entrained to the temperature cycle, with sleep efficiency (TST/Total Bed Time) being maximal when temperature was lowest. While temperature is closely related to the ability to fall asleep and remain asleep, several other factors appear to influence the sleep stages. The relationships of the sleep stages from one nap to the next differed from their hour-to-hour relationships on the baseline night. The reciprocal positive relation between stage 4 and stage REM appears to be unique to naps. In monophasic nocturnal sleep, stage REM regulated itself from one hour to the next, and was independent of the amount of stage 4 in a preceding or subsequent hour. In contrast to the REM alternation reported by Carskadon and Dement (1975), in our study, REM did not predict itself from one nap to the next. The waking period between naps apparently facilitated the stage 4-stage REM feedback since such feedback did not exist in continuous sleep. On the other hand, the waking period interfered with the self-regulation of stage REM, since the negative feedback observed in nocturnal continuous sleep did not occur in naps. Ephron and Carrington (1966) and Berger (1969) have hypothesized that the function of REM sleep is to increase cortical and oculomotor activity during sleep. The assumption is that during sleep, periodic activation of these systems to waking levels is necessary for efficient functioning during the subsequent waking state. Freemon (1972, p. 152) stated the REM activation hypothesis as "each rem period could be replaced by a period of wakefulness". This hypothesis is clearly refuted by the fact that waking periods between naps do not inhibit or substitute for REM sleep. As noted earlier, it has been suggested that the 90-110 min REM cycle in sleep continues to operate with the same periodicity throughout the waking state (a sleep-independent clock): 90-110 min cycles have been found in arousal level, gastric motility, and some hormone secretions. Although a thorough analysis and
632
J.M. MOSESet al.
discussion of the ultradian REM cycle clock are Total sleep time and the amount of stage not intended for this report, the results of our REM during the naps were negatively related to REM cycle analysis indicate that the clock the circadian-temperature cycle. Stage REM governing the REM cycle is sleep-dependent-- frequently appeared within 10 min of stage 1 it stops upon awakening and resumes at the next onset and the normal sequence of stages REM sleep onset. This suggests that the 90-110 rain and 4 were altered, demonstrating that the cycles found in the awake subject are not ex- organization of sleep within a nap is quite differpressions of the 90-110 min REM cycle found ent from that in monophasic nocturnal sleep. during sleep. Auto-correlation and cross-correlation analyses Although TST during the 10 naps was lower showed that the relation of sleep stages from than baseline, the relatively small amount of hour to hour in normal continuous baseline sleep sleep loss incurred by napping was not sufficient was altered in nap-to-nap comparison. The to produce the changes in recovery sleep timing of REM onset may be controlled by a usually associated with sleep loss. But the reco- sleep-dependent ultradian clock; the clock may very night for the Ex group looked much like stop upon awakening and resume at the next sleep typical recovery sleep following sleep loss of 1-2 onset. Naps had recuperative value in terms of nights. Shorter sleep latencies, reduced W time, maintaining the normal amounts of sleep stages and greatly augmented stage 4 were present. on the recovery night; recovery sleep for the Because no such differences were found be- exercise group showed typical sleep-loss effects. tween baseline and recovery for the Nap group, naps presumably have some recuperative value, RESUME at least in terms of preserving the normal amounts DYNAMIQUE DU SOMMEIL DE SIESTE AU COURS and distribution of sleep stages during recovery D'UNE PERIODE DE 4 0 HEURES sleep. The length of time the subject is on the nap sleep regime, however, seems to be impor- Apr~s une nuit de contr61e, le sommeil de 8 tant in determining sleep patterns on the recovery sujets mfiles adultes r6parti en siestes d'une heure, night. In the Weitzman et al. (1974) and Carska- 6galement espac6e au cours d'une p6riode de don and Dement (1975) studies, subjects were 40 h, est explor6. 10 sujets additionnels ont 6t6 maintained on the nap sleep schedule much privds de sommeil pendant 40 h avec des p6riodes longer (10 and 5 days repectively) than the 40 h d'une heure d'exercice donn6es fi la place des of the present study, and both of those studies siestes. Une nuit de r6cup6ration suit la p6riode reported sleep-deprivation effects on the reco- de 40 h pour les deux groupes. very nights. Le temps de sommeil total et la quantit6 de Sleep during naps cannot be accounted for sommeil paradoxal au cours des siestes est en exclusively within the framework of what we liaison n6gative avec le cycle circadien de la temknow about monophasic nocturnal sleep. The p6rature. Le sommeil paradoxal apparait fr6results of this study show that no single factor quemment au cours des 10 premi6res rain de Fendetermines the type of sleep that will occur in a dormissement en stade I, et la s6quence normale, given nap, and the hypotheses put forth to de sommeil paradoxal et de stade IV est alt6r6e, explain the dynamics of nap sleep overlap montrant que l'organisation du sommeil considerably. l'int6rieur d'une sieste est tout fi fait diff6rente de ce qu'elle est dans le sommeil nocturne SUMMARY monophasique. Des analyses d'auto-corr61ation et de cross-corr61ation montrent que la relation Following 1 baseline night, the sleep of 8 adult des stades du sommeil d'heure en heure au cours males in equally spaced 1 h naps during a 40 h du sommeil normal continu lors de la nuit de period was examined. Ten additional subjects contr61e est alt6r6e dans les s6quences comparawere sleep-deprived for 40 h with 1 h periods of tives sieste-~t-sieste. On peut penser que la exercise given in place of naps. One recovery survenue temporelle de l'endormissement en night followed the 40 h period for both groups. sommeil paradoxal est contr616e par une horloge
NAP SLEEP DYNAMICS
ultradienne d~pendant du sommeil ; cette horloge peut s'arr&er lors de l'6veil et reprendre au prochain endormissement. Les siestes ont une valeur r6paratoire en ce sens qu'elles maintiennent les quantit6s normales de stades de sommeil au cours de la nuit de r6cup6ration" le sommeil, lors de la nuit de r6cup6ration dans le groupe qui a subi les exercices montre les effets typiques de manque de sommeil. REFERENCES BERGER, R. J. Oculomotor control: a possible function of REM sleep. Psychol. Rev., 1969, 76: 144-164. CARSKADON,M. A. and DEMENT, W. C. Sleep studies on a 90-minute day. Electroenceph. clin. Neurophysiol.. 1975, 39: 145-155. EPHRON, H. S. and CARRINGTON,P. Rapid eye movement sleep and cortical homeostasis. Psychol. Rer.. 1966, 73: 500-526. FREEMON, F. R. Sleep research. Thomas, Springfield, Ill.. 1972, 205 p. GLOBUS, G. G. Rapid eye movement cycle in real time. Arch 9en. Psychiat., 1966, 15: 654-659. HORD, D. Common mode rejection techniques in conjugate eye movement recording during sleep. Psychophysioloqy, 1975, 12: 354-355. KELLEY, J., LAUGHLIN, E., CARPENTER, S., SIMMONS, J.. SIDORIC, K. and LENTZ, R. A study of ninety-minute sleep cycles. Stanford Review, 1973, 3: 1-5. KENDALL, M. G. and STUART, A. The advanced theory of statistics, VoL HI. Griffin. London, 1966. KLEITMAN, N. Sleep and wakefulness. University of Chicago
633 Press, Chicago, II1., 1%3, 552 p. KRIPKE, D. F. Ultradian rhythms in sleep and wakefulness. In E. D. WEITZMAN (Ed.), Advances in sleep research, Vol. 1. Spectrum Publications, a subsidiary of Wiley, New York, 1974: 305-325. LAVlE, P., LORD, J. W. and FRANK, R. A. Basic rest-activity cycle in the perception of the spiral after-effect: a sensitive detector of a basic biological rhythm. Behar. Biol.. 1974, I1~ 373--379. LUBIN, A., HORD, D. J., TRACY, M. L. and. JOHNSON, L. C. Effects of exercise bedrest and napping on performance decrement during 40 hours. Submitted to Psychophysiology. MOSES, J., LUBIN, A., NAITOH, P. and JOHNSON, L. C. Reliability of sleep measures. Psychophysioloyy, 1972, 9: 78 82. RECHTSCHAFFEN, A. and KALES, A. (Eds.). A manual o/ standardized terminology, techniques and scoring system jor sleep stages of human sut~jects. Public Health Service, U.S. Government Printing Office, Washington, D.C., 1968. SNYDER, F. The new biology of dreaming. Arch. #en. Psychiat., 1963, 8." 381 391. WEBB, W. B. and AGNEW JR., H. W. Sleep cycling within twenty-four hour periods. J. exp. Physiol., 1967, 74: 158-160. WEBB, W. B., AGNEW JR., H, W. and STERNTr~AL, H. Sleep during the early morning. Psychonom. Sci., 1966, 6: 277 278. WEITZMAN,E. D., NOGEIRE,C., PERLOW,M., FUKUSHIMA,D., SASSIN, J., MCGREGOR, P., GALLAGHER,T. F. and HELLMAN, L. Effects of a prolonged 3-hour sleel~wake cycle on sleep stages, plasma cortisol, growth hormone and body temperature in man. J. clin. Endocr., 1974, 38: 1018 1030.