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Recovery within day-time sleep after slow wave sleep suppression
267
Electroencephalography and clinical Neurophysiology, 1991, 7 8 : 2 6 7 - 2 7 3 © 1991 Elsevier Scientific Publishers Ireland, Ltd. 0013-4649/91/$03.50 A D O N I S 0013464991000796
EEG89666
Recovery within day-time sleep after slow wave sleep suppression Mats Gillberg a, Ingrid Anderzrn b and Torbjrrn .~kerstedt a a I P M and Stress Research, Karolinska Institute, S-104 O1 Stockholm (Sweden), and b National Defence Research Establishment, Department 5, S-102 54 Stockholm (Sweden) (Accepted for publication: 12 May 1990)
Summary Six subjects had their SWS activity suppressed by acoustic stimulation during a day-time (11.00 h) recovery sleep after a 4 h night sleep (03.00-07.00 h). Sleep was disturbed for a period corresponding to 90% of the duration of a preceding undisturbed baseline sleep (also at 11.00 h and preceded by a 4 h night sleep) and thereafter allowed to continue undisturbed until spontaneous awakening. The results showed that SWS and EEG power density were significantly reduced during suppression and that full recovery occurred before spontaneous awakening. The disturbed sleep was significantly longer than the baseline sleep. The increase in duration consisted mainly of SWS, stage 2 and REM. The results suggest that the suppression of SWS activity caused a need for an extension of sleep in order to allow recovery.
Key words: SWS deprivation; Power density; Sleep duration; Sleep homeostasis
It has repeatedly been shown that the sleep/wake alternation follows a circadian rhythm. Sleep duration depends on when during the circadian cycle it is initiated (Czeisler et al. 1980; Akerstedt and Gillberg 1981; Zulley et al. 1981). Homeostatic influences after sleep loss on subsequent sleep have been described by, e.g., Webb and Agnew (1971, 1975) and Feinberg et al. (1985, 1987). Recently it has been shown that spectral power density is an extremely sensitive EEG measure of sleep after total sleep loss (Borbrly et al. 1981). In two recent papers (,~kerstedt and Gillberg 1986a, b) we reported that day-time recovery sleep after sleep loss had a clear dose-dependent relation to amounts of preceding nocturnal sleep: total sleep time (TST), stage 2 (St 2), stage 3 + 4 (slow wave sleep; SWS) and spectral power density in the delta + theta band increased as prior nocturnal sleep decreased. If EEG power density reflects a homeostatic process one would predict that a suppression of EEG power density would lead to an increased SWS activity when suppression was discontinued, i.e., to a recovery process within the same sleep. Furthermore, one would expect
t We would like to dedicate this paper to the memory of our friend and colleague Dr. Lars Torsvall who died on the 10th of August 1989. Correspondence to: Mats Gillberg, IPM and Stress Research, Karolinska Institute, S-104 01 Stockholm (Sweden).
sleep not to terminate until recovery of the loss was accomplished. Dijk and Beersma (1989) suppressed power density by acoustically disturbing SWS. They found recovery, i.e., increased delta activity, after cessation of the suppression but failed to observe any change in sleep duration. Their designs involved, for one of the experiments, SWS suppression during the first 5 h of a night-time sleep and, for the other, SWS suppression during the first 3 h of a recovery sleep at 11.00 h after 1 night's loss of sleep. In both cases ad lib. recovery was allowed following the end of the suppressed period. The lack of expected sleep extension may have been due to difficulties in successfully suppressing power density for long periods of time. This may have been particularly difficult after the sizeable sleep loss of the second study. Also, the large proportion of undisturbed sleep after the suppression may have allowed too much recuperation before any sleep extension could occur. Thus approximately 40% of the night-time sleep and 60% of the day sleep was left undisturbed. The present study also focussed on the effect of suppression of SWS on sleep extension but used a design with sleep scheduled to 11.00 h after a preceding night sleep curtailed to only 4 h. This limitation would presumably create enough need for sleep to facilitate falling asleep at 11.00 h without incurring large demands for delta power (Akerstedt and Gillberg 1986a, b). Furthermore, the proportion that was left undisturbed was reduced to 10% (of normal undis-
268
M. G I L L B E R G ET AL.
turbed sleep) in order to prevent complete recovery within the normal period of sleep.
Methods
Six subjects (2 females and 4 males; age range 23-45 years) participated. They all had experience as subjects in studies involving EEG recording of sleep. The subjects had their sleep recorded during 3 day-time sleeps (scheduled to 11.00 h) after night sleeps restricted to 4 h (03.00-07.00 h; see Fig. 1). The purpose of the first of these conditions was to establish the individual spontaneous duration of a sleep that was started at 11.00 h and preceded by a 4 h night sleep. Data from this condition are treated as baseline values. Prior to the following 2 conditions, the subjects were told that their sleep could be disturbed. Actually they were disturbed only during one of the conditions. Half of the subjects started with the disturbed sleep and the other half with the undisturbed. Results from the undisturbed sleep episodes are not reported in the following, since these episodes were merely included to balance out possible effects of expectation. During the disturbed condition each subject had the sleep disturbed for a period corresponding to 90% of the duration (total sleep time; TST) of the baseline sleep. On all occasions the preceding night sleep was restricted to between 03.00 and 07.00 h. The night sleeps were not monitored, but the subjects were instructed to adhere strictly to the timing of bedtime and awakening. The recorded sleep episodes were scheduled to 11.00 h and the subjects arrived at the laboratory at 09.00 h for preparation and application of electrodes. They were also given a small snack. The laboratory was isolated
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from external time cues and the subjects slept individually in comfortable darkened bedrooms. Sleep was on all occasions terminated by spontaneous awakening. During the disturbed condition SWS activity was suppressed by acoustic stimulation. The experimenter continuously monitored the EEG chart and delivered a tone by pressing a button whenever SWS activity occurred. The tone could be varied in duration, frequency (50-1000 Hz) and volume (70-85 dBA). SWS activity was defined as any occurrence of delta activity (0 4 Hz: > 75 #V). After cessation of the disturbance the subjects were left to sleep until spontaneous awakening. EEG (Cz-Pz) and EOG were recorded continuously on portable EEG tape recorders (Medilog '~ equipment) and simultaneously on paper. Paper records were conventionally scored {30 sec epochs, chart speed 10 m m / s e c ) according to Rechtschaffen and Kales (1968). Standard abbreviations of stages are used throughout the text. The tape records were later subjected to frequency analysis (FFT; Torsvall et al. 1984) of artifact-free 7.5 sec epochs, later averaged to form 1 min intervals. Power densities were integrated over the 0.5 3.9 Hz (delta), 4 -7.9 Hz (theta) frequency bands as well as over the 0.5 ~16 Hz band and accumulated over the time periods of interest for stages 1 + 2, SWS, REM and total sleep, respectively. In addition, power densities per minute were calculated for the same frequency bands, periods and stages. Power density data were expressed relative to the accumulated power density of all stages at awakening from the baseline sleep (100%) and to the mean power d e n s i t y / m i n of baseline sleep (100%), respectively. Also the time axis was expressed relative to the duration of the baseline sleep (100%). Epochs with stage 0 and movement time (MT) were removed from the power density data. All comparisons were made within subjects. The Wilcoxon matched pairs signed ranks test (Siegel 1959) was used for all analyses since durations and F F T power density data were expressed relative (%) to the baseline condition. Hence, distributions could not be expected to be normal.
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Fig. 1. The design of the study, All 3 conditions included a 4 h night sleep. The first condition included a baseline day-time sleep for all subjects. The second condition included a disturbed day-time sleep for 3 subjects (A) and undisturbed for the other 3 (B). During the third condition the order was reversed. A and B denote the 2 groups. The undisturbed sleep episodes are not used in the analyses.
Fig. 2 shows the effects on the timing and duration of sleep stages. The first cycle of the disturbed sleep deviated from that of the baseline sleep mainly through the marked loss of SWS. The second cycle of the disturbed sleep was for all subjects started before the cessation of disturbance. Five of the 6 subjects had at least 2 complete cycles during the disturbed sleep. The process of accumulation of relative delta power density during the 2 conditions is plotted against relative time in Fig. 3. The initial increase in rate of accumulation seen for the baseline data is absent for the
RECOVERY AFTER SWS SUPPRESSION
269
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RELATIVE DURATION ( % of baseline sleep ) Fig. 2. Timing and duration of sleep stages (stages 1 + 2, SWS, and REM sleep) during baseline and disturbed sleep for each of the 6 subjects. Time is expressed relative to the duration of the baseline sleep ( = 100%). Vertical arrow at 90% marks the cessation of disturbance during disturbed sleep and the corresponding time during baseline sleep. For tests of significance,see Table 1.
d i s t u r b e d sleep. I m m e d i a t e l y following the cessation of d i s t u r b a n c e there was a significantly faster rate of accum u l a t i o n c o m p a r e d to the c o r r e s p o n d i n g period of the baseline sleep: the change in power density (i.e., the slopes of the curves) from 90% to 100% of time was significantly larger (steeper slope) for d i s t u r b e d sleep ( P < 0.05, W i l c o x o n m a t c h e d pairs signed r a n k s test of the difference b e t w e e n conditions). A c o m p a r i s o n with Fig. 2 shows that the steep part of the baseline sleep curve coincides with the SWS periods in the first baseline cycle while the steep part of the d i s t u r b e d sleep curve shows a similar c o n n e c t i o n with SWS periods d u r i n g the second cycle of the d i s t u r b e d sleep. As the d i s t u r b e d sleep exceeded baseline sleep i n d u r a t i o n there were n o longer a n y significant differences in a c c u m u l a t e d power densities b e t w e e n the 2
sleep c o n d i t i o n s : neither at 110%, 120%, 130% of time n o r at sleep t e r m i n a t i o n did a c c u m u l a t e d power d e n s i t y d u r i n g the d i s t u r b e d sleep differ significantly from the final level reached d u r i n g the baseline sleep. T h e results for d u r a t i o n s of stages are shown in T a b l e I. Both the baseline a n d the d i s t u r b e d sleeps were analysed in 2 parts. T h e first interval was 90% of the d u r a t i o n of the baseline sleep or the d i s t u r b e d period of the d i s t u r b e d sleep a n d the second interval was the r e m a i n i n g 10% of the baseline sleep or the recovery period of the d i s t u r b e d sleep. Also c o m p a r i s o n s b e tween the total sleep periods are presented. Stages 3 a n d 4 (and SWS) were significantly reduced d u r i n g the d i s t u r b e d period, whereas there were significant increases of stage 2 a n d of w a k i n g (stage 0). T h e recovery period of the d i s t u r b e d sleep was significantly
TABLE 1 Visually scored sleep parameters during the 90% of B sleep/disturbed period, the remaining 10%/recovery period and for the total sleep periods. Sleep parameter
90% of B sleep/disturbed period B sleep D sleep
Remaining 10%/recovery period B sleep D sleep
Total sleep B sleep
D sleep
Stage 0 Stage 1 Stage 2 Stage 3 Stage 4 SWS REM MT TST
2.8 (0.7) 11.8 (3.8) 45.6 (4.8) 11.3 (2.0) 13.0 (3.3) 24.3 (4.6) 21.3 (5.5) 1.8 (1.0) 105.0 (8.4)
0.8 (0.4) 3.1 (1.0) 4.9 (1.8) 1.4 (1.4) 0.5 (0.5) 1.9 (1.9) 1.2 (1.2) 0.6 (0.3) 11.9 (1.1)
3.6 14.9 50.5 12.8 13.5 26.3 22.5 2.4 116.9
15.7 (5.3) * 24.8 (4.7) 93.8 (18.1) * * 8.8 (2.4) 16.3 (5.9) 25.0 (7.8) 32.7 (8.4) 3.9 (1.4) 180.2 (25.6) * *
Stage 1 latency REM latency
7.8 (2.7) * 18.3 (3.8) 59.3 (7.7) * 3.8 (1.7) ** 1.0 (0.7) * 4.8 (2.3) ** 20.2 (7.2) 2.3 (1.2) 105.0 (8.4)
4.8 (2.2) 6.5 (1.8) 34.5 (11.1) * 5.0 (1.0) 15.3 (5.9) 20.3 (6.7) * 12.5 (2.9) * 1.6 (0.6) 75.2 (18.9) * *
(1.0) (2.7) (6.0) (2.8) (3.4) (5.6) (4.7) (1.2) (9.4)
13.33 (8.9) 71.4 (6.6)
3.9 (0.7) 67.4 (10.3)
Figures represent means and standard errors (within parentheses) in minutes. Asterisks denote significant differences between baseline (B sleep) and disturbed sleep (D sleep) conditions for corresponding periods. Wilcoxon test * * < 0.03, * < 0.05, n = 6.
270
M. GILLBERG ET AI,.
FABLE II Relative power density in frequency bands during sleep stages for 90% of B sleep/disturbed period, the remaining 10%/recovery period and for the complete sleep periods. All values expressed as % of total power of baseline sleep ( = 100%). Sleep param,
Frequency band
90% of B sleep/disturbed period
Remaining 10%/recovery period
Total sleep
B sleep
D sleep
B sleep
D sleep
B sleep
St 1 +2
delta theta tot. (0.5-16 Hz)
22.5 (3.9) 7.4(1.1) 38.2 (6)
31.3 (4.4) ** 9.4(1.4) ** 50.4 (6.6) *
4.1 (l.1) 1.2(0.41 6.9 (1.9)
18.2(4.8) ** 5.0(1.3) ** 29.(I (7.6) * *
26.6 (4.l) 8.6(1.41 45.1 (6.9)
49.5 (7.1) ** 14.4(2.31 ** 79.4 (11.7~ * *
SWS
delta theta tot. (0.5 ~ 16 Hzl
33.6 (6.6) 19.5 (2.4) 41.0 (6.9)
only 2 subj. with SWS
only 1 sut~j. with SWS
27.9 (9,2) 2.(~ (0.8) 32.7 (10.6~
35.6 (7.3) 3.9 (0.4) 43,4 (7.7)
_?0,,~ (9.6~ 3.0 (0.9~ 36.3 (11 2/
REM
delta theta tot. (0.5-16 Hz)
5.6 (1.31 2.4 (0.61 10.4(2.4)
4.8 (1.4) 1.9 t0.61 8.5(2.6)
only t subj. with REM
3.5 (0.8) 1.3 (0.3) 6,1(1.41
6.3 (0.8) 2.6 (0.4) 11.5(1.5)
8.3 (1.61 3.2 (0.7) 14.6 (2.8)
All stages
delta theta tot.(0.5 16 Hz)
61.7(3.5) 13.5(l.1) 89.7(1.21
39.1 (4.7) * 11,7(1.51 62.5(6.9) **
6.7(1.21 1.610.31 10.3(1.21
49.7(11.51 ** 8.9 (1.81 ** 66.5(14.9) **
68.4(3.7) 15.1 (1.31 11141 (basel.)
D sleep
88.8 (t2,91 20.6 (2,5) * 129.0(16.51
Figures represent means and standard errors (within parentheses) in percent. Asterisks denote significant differences between baseline (B sleep) and disturbed sleep (D sleep) conditions for corresponding periods. Wilcoxon test * * < 0.03. * < 0,05: n ~ 6. Figures in italics derive from 5 subjects (1 subject lacked SWS and 1 subject lacked REM).
longer than the corresponding period during baseline sleep and contained significantly more stage 2, SWS, and REM while there were no significant differences for stages 0, 1, and MT. The disturbed sleep was significantly longer (TST; 51% _+ 12%; Wilcoxon, P < 0.03) than the baseline sleep. Also stages 0 and 2 differed significantly between the 2
conditions. Stage 1 latency and REM latency did not differ significantly, neither did the duration of the first cycle (defined as the time from onset of stage 1 to end of REM: see Table IV). Baseline sleep contained only one complete sleep cycle whereas the disturbed sleep contained at least two cycles for all subjects except one (see Table IV).
TABLE 11I Relative power density per minute in frequency bands during sleep stages for 90% of B sleep/disturbed period~ the remaining 10%/recovery period and for the total sleep periods. All values expressed as % of total power density per minute of baseline sleep ( 100%), Sleep param,
Frequency band
90% of B sleep/disturbed period
Remaining 10%/recovery period
I otal sleep
St 1 + 2
delta theta tot. (0.5 16 ttz)
B sleep
B sleep
B sleep
SWS
delta theta tot.(0.5 16 Hz)
157.7 (12.8) 19.5 (2.4) 197.2(13.51
REM
delta theta tot. (0.5-16 Hz)
All stages
delta theta tot.(0.5--16 Hz)
43.3 (5) 14.5 ( 1 . 7 1 73.8 (7.6)
D sleep 47.0(6.1) 14.1(2.11 75.4 (9.3)
D sleep
52.0(10.61 14.8 (3.7) 88.9 (17.1)
59.8(10,71 16.1 (2,5) 91.l (14.8)
only 2 subj. withSWS
only 1 subj. withSWS
/3&5 (29.21 14.0 (3.7j ~ 165.8(34. o~
27.7 (6.2) 11.5 (2.5) 51.6(11.61
32.2(4.2) 12.2(1.4) 56.0(7.11
only l subj. with REM
2&9 (6.4) 10.8 (2.5) 49.8(ll.2)
68.0 (4.0) 14.8 ( 1 . 3 1 98.7 (1.6)
43.4(5.2)** 13.1(1.71 71.5 (7.8) **
65.7(11.8) 16.0 (2.2) 101.4(10.71
81.8(15.61 ~ 15.1 (1.81 110.8(17,01 ~
45.4 (4.6) 14.7 (1.81 76,7 (7.4) 156.6 (12.6) 19.5 (2.4) 196.(1(13.5)
D sleep 46.1 (8) 13.3 (2.5) 73.5 (12.6) 15Z1 (12.4) 17.3 (2,6)* 18Q.O(lS.I)
~7.0 (4.8) i4.7 (1.31 67.5 (7.7)
33.3 (3.4) 12.5 (l 3) 57.8 (6.1)
68.4 (3.7) 15.1 (1.31 I00 (baseline)
58.6 (0.8) 13.8 (17l 86.5 (10.t)
Figures represent means and standard errors (within parentheses) in percent. * denote significant differences between baseline (B sleep) and disturbed sleep (D sleep) conditions, t denote differences between the 90% of B sleep and remaining t0% or disturbed period and recovery period. § denote differences between the recovery period of D sleep and the first 90% of B sleep. Wilcoxon test * *'tt < 0.03; .,t,§ < 0.05: n = 6. Figures in italics derive from 5 subjects (1 subject lacked SWS and 1 subject lacked REM).
271
R E C O V E R Y A F T E R SWS SUPPRESSION
The accumulated power density (Table II) was significantly reduced during the disturbed period compared to the co~responding period of the baseline sleep. The reduction was mainly in the delta band. The recovery period contained significantly more power density in all frequency bands than the corresponding period of baseline sleep. At the termination of the disturbed sleep there were no significant differences from baseline power density. The disturbed sleep contained significantly more delta, theta and total (0.5-16 Hz) power in stage 1 + 2 during both the disturbed and the recovery periods compared to the baseline sleep. Significant differences in the same direction were found also when the complete sleep periods were compared. Table III shows the intensity dimension of the power density data, i.e., relative power density per minute. Tests of significance were made for differences between conditions for the 90% of baseline/disturbed period, the remaining 10% of baseline/recovery period, and the total sleep periods, respectively, as well as between the disturbed and recovery periods and between the first 90% and the remaining 10% of baseline sleep. Also the recovery period was tested against the first 90% of the baseline sleep. The disturbed sleep was found to be slightly, but significantly, less intense in the theta band during SWS than the baseline sleep. The disturbed period was less intense than the corresponding period of the baseline sleep. The data show that it is mainly delta activity that is responsible for this difference. During the recovery period there were no significant differences
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T A B L E IV Sleep cycles: relative power density in frequency bands, durations, and n u m b e r of complete cycles.
Frequency band Delta Theta Tot. (0.5-16 Hz) Duration of cycle (min) No. of subjects with complete cycle
1st cycle B sleep
1st cycle D sleep
2nd cycle D sleep
69.7 (3.6) 15.1 (1.4) 100 (baseline)
37.0 (6.3) * * 11.8 (2.5) * 60.5 (10.7) * *
50.2 (10.8) 11.2 (2.6) 71.7 (1.4)
87.3 (10.3)
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Relative power in percent of total power for the first cycle of baseline sleep. Asterisks denote significant differences between 1st cycle of baseline sleep (B sleep) and 1st cycle of disturbed sleep (D sleep). Wilcoxon test * * < 0.03, *0.05; n = 6. Figures in italics derive from 5 subjects.
in sleep intensity from the corresponding period of the baseline sleep. Comparing the disturbed period with the recovery period, delta intensity as well as total intensity were significantly higher during the latter. SWS theta activity was slightly less intense during the recovery period than during the first 90% of the baseline sleep. Table IV shows power density data analysed for sleep cycles. (A Friedman non-parametric ANOVA, which would have been the appropriate test, could not be used since only 5 subjects had a second cycle.) The first cycle of the disturbed sleep contained significantly less power density than that of the baseline sleep for the delta and theta bands as well as for all bands together. The duration of the first cycle did not differ between conditions.
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RELATIVE TIME ( % of baseline ) Fig. 3. Accumulation of relative delta E E G power density for baseline and disturbed sleep over relative time. Power is expressed relative to the total amount accumulated during the baseline condition ( = 100%) and time relative to the duration of the baseline sleep (=100%). Means and standard errors, n = 6. Asterisks denote significant differences ( P < 0.05, Wilcoxon) between baseline and disturbed sleep, ns denotes non-significant differences from the baseline finishing power value, i.e., 100%. Accumulation was done by adding the means of successive 10% time intervals. The curve describing disturbed sleep is continued for as long as all subjects (n = 6) are asleep. The single symbol (open square) shows mean relative power at awakening plotted against mean relative duration for the disturbed sleep ( + 1 S.E.)
Slow wave sleep and E E G power density (especially in the delta band) were clearly suppressed by the acoustic stimulation. This effect was achieved with only slightly increased amounts of waking. Recovery was characterized by a prolongation of sleep. The increased sleep time contained mainly SWS, stage 2 and REM sleep. The results are similar to the observations of Dijk and Beersma (1989) in that suppression of delta activity led to a displacement of SWS and delta power density from their normal positions early in sleep to the latter part of sleep which had been left undisturbed. In contrast to their study, however, we obtained a very clear prolongation of sleep for the baseline condition. The reason that we were able to demonstrate this effect in our study was probably that our period of suppression
272 covered a p e r i o d c o r r e s p o n d i n g to 90% of the d u r a t i o n of the baseline sleep, leaving very little time for recovery within the n o r m a l l y expected sleep d u r a t i o n . T h u s any recovery of SWS (delta) activity would have to be a c c o m p l i s h e d via a p r o l o n g a t i o n of sleep. In the study by D i j k a n d Beersma (1989), on the other hand, the length of the suppression p e r i o d c o n s t i t u t e d only 63% a n d 50%, respectively, of the d u r a t i o n of control sleep, leaving time for c o n s i d e r a b l e recovery of the loss within the time span c o r r e s p o n d i n g to the u n d i s t u r b e d sleep condition. The rate of E E G p o w e r a c c u m u l a t i o n increased after cessation of disturbance. Since S W S contains con~idera b l y m o r e delta p o w e r d e n s i t y than other stages the increased rate of a c c u m u l a t i o n can be a t t r i b u t e d m a i n l y to the a p p e a r a n c e of SWS. (The significant differences in total delta intensity presented in T a b l e I I I can be e x p l a i n e d by the a b s e n c e of S W S d u r i n g the d i s t u r b e d p e r i o d and its presence d u r i n g the recovery period.} U n e x p e c t e d l y , there were no significant increases in delta intensity d u r i n g SWS or stage 1 + 2. If the supp r e s s i o n h a d created a " p r e s s u r e " specifically for delta activity, such an increase might have been expected. On the o t h e r hand, the level of pressure for S W S b r o u g h t a b o u t by the p r e s e n t design might, however, have been too low to stimulate an increase in S W S (delta) intensity. W h e n the s p o n t a n e o u s a w a k e n i n g occurred, the loss of S W S a n d delta p o w e r density h a d recovered completely. Stage 2 ( a n d p o w e r d e n s i t y of stage 1 + 2), however, " o v e r - r e c o v e r e d . " It increased d u r i n g recovery in spite of the fact that it had even increased signific a n t l y d u r i n g the d i s t u r b e d period. This finding argues against stage 2 a m o u n t s being i m p o r t a n t for recovery. Also R E M sleep showed a t e n d e n c y to over-recover d e s p i t e the lack of any loss during the d i s t u r b e d period. In fact, a p p r o x i m a t e l y 2 / 3 of the sleep extension consisted of stages 2 a n d R E M whereas only 1 / 3 consisted of SWS. W h a t then, was the reason for the extension of stages 2 a n d R E M ? W e suggest that the S W S deficit at the t r a n s i t i o n between the first a n d s e c o n d cycles acted as a p r o m p t to ensure a full second cycle with a n o r m a l structure, i.e., with initial stage 2 a n d a final R E M sleep period, and with the S W S p e r i o d in between. Thus, the second cycle and its c o n t e n t of stages 2 a n d R E M w o u l d be seen as the vehicle for S W S (delta) recovery. This would, again, suggest that stage 2 a n d R E M or their c o n t e n t of d e l t a activity lack h o m e o s t a t i c or recuperative value b y themselves. T h e present data, however, give only weak s u p p o r t for such an i n t e r p r e t a t i o n . S t r o n g e r evidence would have been if all stage 2 activity h a d p r e c e d e d S W S d u r i n g the recovery period. The a b o v e o b s e r v a t i o n s also attest to the r e m a r k a b l e resistance of R E M sleep. A l t h o u g h S W S was being suppressed, a R E M p e r i o d a p p e a r e d with the same
M. GILLBERG ET Air. latency a n d d u r a t i o n as that of baseline sleep. A similar resistance was o b s e r v e d b y ourselves in a recent study ( G i l l b e r g a n d A,kerstedt 1991) where we f o u n d the process of S W S (delta) recovery after total sleep loss to be i n t e r r u p t e d b y R E M sleep a n d c o n t i n u e d d u r i n g the second sleep cycle after an initial p e r i o d of stage 1 + 2 sleep. T h e latter f i n d i n g also s u p p o r t s the i n t e r p r e t a t i o n of the increased sleep d u r a t i o n in the p r e s e n t s t u d y as p a r t l y a c o n s e q u e n c e of the cyclic structure of sleep: lost S W S is m a i n l y recovered d u r i n g the regular S W S period, after the n o r m a l sequence of o t h e r stages. In conclusion, the p r e s e n t s t u d y has d e m o n s t r a t e d that s u p p r e s s i o n of S W S (delta) activity for a d u r a t i o n c o r r e s p o n d i n g to that of a n o r m a l s p o n t a n e o u s l y t e r m i n a t e d sleep will cause p r o l o n g a t i o n of sleep in o r d e r to recover the a m o u n t s lost. A direct i n t e r f e r e n c e with the S W S (delta) process starts a recovery process that is similar to that after total sleep d e p r i v a t i o n . We would like to thank G6ran Ekstr6m, GiSran Lindbeck, Karin Sigurdson and GiSran Stensson for help with data collection.
References
~,kerstedt, T. and Gillberg, M. The circadian variation of experimentally displaced sleep. Sleep, 1981, 4: 159-169. ,~kerstedt, T. and Gillberg, M. A dose-response study of sleep loss and spontaneous sleep termination. Psychophysiology, 1986a, 23: 293-297. Akerstedt, T. and Gillberg, M. Sleep duration and the power spectral density of EEG. Electroenceph. clin. Neurophysiol., 1986b, 64: 119-122. Borbdly, A.A., Bauman, t:., Brandeis, D., Strauch, 1. and Lehmann, D. Sleep deprivation: effect on sleep stages and EEG power density in man. Electroenceph. clin. Neurophysiol., 1981, 51: 483-493. Czeisler, C.A., Weitzman, E.D., Moore-Ede, M.C., Zimmerman, J.C. and Knauer, R.S. Human sleep: its duration and organization depend on its circadian phase. Science, 1980, 210: 1264-1267. Dijk, D.J. and Beersma, D.c.M. Effects of SWS deprivation on subsequent EEG power density and spontaneous sleep duration. Electroenceph. clin. Neurophysiol., 1989, 72: 312-320. Feinberg, I., March, JD.. Floyd, T.C., Jimison, R., Bossom-Demitrack, L. and Katz, P.H. Homeostatic changes during post-nap sleep maintain baseline levels of delta EEG. Electroenceph. clin. Neurophysiol., 1985, 61: 134-137. Feinberg, I.. Floyd, T.C., and March, J.D. Effects of sleep loss on delta (0.3-3 Hz) EEG and eye movement density: new observations and hypothesis. Electroenceph. clin. Neurophysiol., 1987, 67: 217--221. Gillberg, M. and ,~kerstedt, T. The dynamics of the first sleep cycle. Sleep, 1991, in press. Rechtschaffen, A. and Kales, A.A. A Manual of Standardized Terminology, Techniques, and Scoring System for Sleep Stages of Human Subjects. U.S. Government Printing Office, Washington, DC, 1968. Siegel, S. Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York, 1959. Torsvall, T., ~,kerstedt, T. and Lindbeck, G. Effects on sleep stages and EEG power density of different degrees of exercise in fit subjects. Electroenceph. clin. Neurophysiol., 1984, 57: 347-353.
RECOVERY AFTER SWS SUPPRESSION Webb, W.B. and Agnew, H.W. Stage 4 sleep: influence of time course variables. Science, 1971, 174: 1354-1356. Webb, W.B. and Agnew, H.W. The effects on subsequent sleep of an acute restriction of sleep length. Psychophysiology, 1975, 12: 367370.
273 Zulley, J., Wever, R. and Aschoff, J. The dependence of onset and duration of sleep on the circadian rhythm of rectal temperature. Pfliigers Arch. Ges. Physiol., 1981, 391: 314-318.
Electroencephalography and clinical Neurophysiology, 1991, 7 8 : 2 6 7 - 2 7 3 © 1991 Elsevier Scientific Publishers Ireland, Ltd. 0013-4649/91/$03.50 A D O N I S 0013464991000796
EEG89666
Recovery within day-time sleep after slow wave sleep suppression Mats Gillberg a, Ingrid Anderzrn b and Torbjrrn .~kerstedt a a I P M and Stress Research, Karolinska Institute, S-104 O1 Stockholm (Sweden), and b National Defence Research Establishment, Department 5, S-102 54 Stockholm (Sweden) (Accepted for publication: 12 May 1990)
Summary Six subjects had their SWS activity suppressed by acoustic stimulation during a day-time (11.00 h) recovery sleep after a 4 h night sleep (03.00-07.00 h). Sleep was disturbed for a period corresponding to 90% of the duration of a preceding undisturbed baseline sleep (also at 11.00 h and preceded by a 4 h night sleep) and thereafter allowed to continue undisturbed until spontaneous awakening. The results showed that SWS and EEG power density were significantly reduced during suppression and that full recovery occurred before spontaneous awakening. The disturbed sleep was significantly longer than the baseline sleep. The increase in duration consisted mainly of SWS, stage 2 and REM. The results suggest that the suppression of SWS activity caused a need for an extension of sleep in order to allow recovery.
Key words: SWS deprivation; Power density; Sleep duration; Sleep homeostasis
It has repeatedly been shown that the sleep/wake alternation follows a circadian rhythm. Sleep duration depends on when during the circadian cycle it is initiated (Czeisler et al. 1980; Akerstedt and Gillberg 1981; Zulley et al. 1981). Homeostatic influences after sleep loss on subsequent sleep have been described by, e.g., Webb and Agnew (1971, 1975) and Feinberg et al. (1985, 1987). Recently it has been shown that spectral power density is an extremely sensitive EEG measure of sleep after total sleep loss (Borbrly et al. 1981). In two recent papers (,~kerstedt and Gillberg 1986a, b) we reported that day-time recovery sleep after sleep loss had a clear dose-dependent relation to amounts of preceding nocturnal sleep: total sleep time (TST), stage 2 (St 2), stage 3 + 4 (slow wave sleep; SWS) and spectral power density in the delta + theta band increased as prior nocturnal sleep decreased. If EEG power density reflects a homeostatic process one would predict that a suppression of EEG power density would lead to an increased SWS activity when suppression was discontinued, i.e., to a recovery process within the same sleep. Furthermore, one would expect
t We would like to dedicate this paper to the memory of our friend and colleague Dr. Lars Torsvall who died on the 10th of August 1989. Correspondence to: Mats Gillberg, IPM and Stress Research, Karolinska Institute, S-104 01 Stockholm (Sweden).
sleep not to terminate until recovery of the loss was accomplished. Dijk and Beersma (1989) suppressed power density by acoustically disturbing SWS. They found recovery, i.e., increased delta activity, after cessation of the suppression but failed to observe any change in sleep duration. Their designs involved, for one of the experiments, SWS suppression during the first 5 h of a night-time sleep and, for the other, SWS suppression during the first 3 h of a recovery sleep at 11.00 h after 1 night's loss of sleep. In both cases ad lib. recovery was allowed following the end of the suppressed period. The lack of expected sleep extension may have been due to difficulties in successfully suppressing power density for long periods of time. This may have been particularly difficult after the sizeable sleep loss of the second study. Also, the large proportion of undisturbed sleep after the suppression may have allowed too much recuperation before any sleep extension could occur. Thus approximately 40% of the night-time sleep and 60% of the day sleep was left undisturbed. The present study also focussed on the effect of suppression of SWS on sleep extension but used a design with sleep scheduled to 11.00 h after a preceding night sleep curtailed to only 4 h. This limitation would presumably create enough need for sleep to facilitate falling asleep at 11.00 h without incurring large demands for delta power (Akerstedt and Gillberg 1986a, b). Furthermore, the proportion that was left undisturbed was reduced to 10% (of normal undis-
268
M. G I L L B E R G ET AL.
turbed sleep) in order to prevent complete recovery within the normal period of sleep.
Methods
Six subjects (2 females and 4 males; age range 23-45 years) participated. They all had experience as subjects in studies involving EEG recording of sleep. The subjects had their sleep recorded during 3 day-time sleeps (scheduled to 11.00 h) after night sleeps restricted to 4 h (03.00-07.00 h; see Fig. 1). The purpose of the first of these conditions was to establish the individual spontaneous duration of a sleep that was started at 11.00 h and preceded by a 4 h night sleep. Data from this condition are treated as baseline values. Prior to the following 2 conditions, the subjects were told that their sleep could be disturbed. Actually they were disturbed only during one of the conditions. Half of the subjects started with the disturbed sleep and the other half with the undisturbed. Results from the undisturbed sleep episodes are not reported in the following, since these episodes were merely included to balance out possible effects of expectation. During the disturbed condition each subject had the sleep disturbed for a period corresponding to 90% of the duration (total sleep time; TST) of the baseline sleep. On all occasions the preceding night sleep was restricted to between 03.00 and 07.00 h. The night sleeps were not monitored, but the subjects were instructed to adhere strictly to the timing of bedtime and awakening. The recorded sleep episodes were scheduled to 11.00 h and the subjects arrived at the laboratory at 09.00 h for preparation and application of electrodes. They were also given a small snack. The laboratory was isolated
NIGHT SLEEP
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from external time cues and the subjects slept individually in comfortable darkened bedrooms. Sleep was on all occasions terminated by spontaneous awakening. During the disturbed condition SWS activity was suppressed by acoustic stimulation. The experimenter continuously monitored the EEG chart and delivered a tone by pressing a button whenever SWS activity occurred. The tone could be varied in duration, frequency (50-1000 Hz) and volume (70-85 dBA). SWS activity was defined as any occurrence of delta activity (0 4 Hz: > 75 #V). After cessation of the disturbance the subjects were left to sleep until spontaneous awakening. EEG (Cz-Pz) and EOG were recorded continuously on portable EEG tape recorders (Medilog '~ equipment) and simultaneously on paper. Paper records were conventionally scored {30 sec epochs, chart speed 10 m m / s e c ) according to Rechtschaffen and Kales (1968). Standard abbreviations of stages are used throughout the text. The tape records were later subjected to frequency analysis (FFT; Torsvall et al. 1984) of artifact-free 7.5 sec epochs, later averaged to form 1 min intervals. Power densities were integrated over the 0.5 3.9 Hz (delta), 4 -7.9 Hz (theta) frequency bands as well as over the 0.5 ~16 Hz band and accumulated over the time periods of interest for stages 1 + 2, SWS, REM and total sleep, respectively. In addition, power densities per minute were calculated for the same frequency bands, periods and stages. Power density data were expressed relative to the accumulated power density of all stages at awakening from the baseline sleep (100%) and to the mean power d e n s i t y / m i n of baseline sleep (100%), respectively. Also the time axis was expressed relative to the duration of the baseline sleep (100%). Epochs with stage 0 and movement time (MT) were removed from the power density data. All comparisons were made within subjects. The Wilcoxon matched pairs signed ranks test (Siegel 1959) was used for all analyses since durations and F F T power density data were expressed relative (%) to the baseline condition. Hence, distributions could not be expected to be normal.
A I UNmTU~D , 11
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TIME OF DAY DURATION, % OF BASE LINE SLEEP
Fig. 1. The design of the study, All 3 conditions included a 4 h night sleep. The first condition included a baseline day-time sleep for all subjects. The second condition included a disturbed day-time sleep for 3 subjects (A) and undisturbed for the other 3 (B). During the third condition the order was reversed. A and B denote the 2 groups. The undisturbed sleep episodes are not used in the analyses.
Fig. 2 shows the effects on the timing and duration of sleep stages. The first cycle of the disturbed sleep deviated from that of the baseline sleep mainly through the marked loss of SWS. The second cycle of the disturbed sleep was for all subjects started before the cessation of disturbance. Five of the 6 subjects had at least 2 complete cycles during the disturbed sleep. The process of accumulation of relative delta power density during the 2 conditions is plotted against relative time in Fig. 3. The initial increase in rate of accumulation seen for the baseline data is absent for the
RECOVERY AFTER SWS SUPPRESSION
269
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RELATIVE DURATION ( % of baseline sleep ) Fig. 2. Timing and duration of sleep stages (stages 1 + 2, SWS, and REM sleep) during baseline and disturbed sleep for each of the 6 subjects. Time is expressed relative to the duration of the baseline sleep ( = 100%). Vertical arrow at 90% marks the cessation of disturbance during disturbed sleep and the corresponding time during baseline sleep. For tests of significance,see Table 1.
d i s t u r b e d sleep. I m m e d i a t e l y following the cessation of d i s t u r b a n c e there was a significantly faster rate of accum u l a t i o n c o m p a r e d to the c o r r e s p o n d i n g period of the baseline sleep: the change in power density (i.e., the slopes of the curves) from 90% to 100% of time was significantly larger (steeper slope) for d i s t u r b e d sleep ( P < 0.05, W i l c o x o n m a t c h e d pairs signed r a n k s test of the difference b e t w e e n conditions). A c o m p a r i s o n with Fig. 2 shows that the steep part of the baseline sleep curve coincides with the SWS periods in the first baseline cycle while the steep part of the d i s t u r b e d sleep curve shows a similar c o n n e c t i o n with SWS periods d u r i n g the second cycle of the d i s t u r b e d sleep. As the d i s t u r b e d sleep exceeded baseline sleep i n d u r a t i o n there were n o longer a n y significant differences in a c c u m u l a t e d power densities b e t w e e n the 2
sleep c o n d i t i o n s : neither at 110%, 120%, 130% of time n o r at sleep t e r m i n a t i o n did a c c u m u l a t e d power d e n s i t y d u r i n g the d i s t u r b e d sleep differ significantly from the final level reached d u r i n g the baseline sleep. T h e results for d u r a t i o n s of stages are shown in T a b l e I. Both the baseline a n d the d i s t u r b e d sleeps were analysed in 2 parts. T h e first interval was 90% of the d u r a t i o n of the baseline sleep or the d i s t u r b e d period of the d i s t u r b e d sleep a n d the second interval was the r e m a i n i n g 10% of the baseline sleep or the recovery period of the d i s t u r b e d sleep. Also c o m p a r i s o n s b e tween the total sleep periods are presented. Stages 3 a n d 4 (and SWS) were significantly reduced d u r i n g the d i s t u r b e d period, whereas there were significant increases of stage 2 a n d of w a k i n g (stage 0). T h e recovery period of the d i s t u r b e d sleep was significantly
TABLE 1 Visually scored sleep parameters during the 90% of B sleep/disturbed period, the remaining 10%/recovery period and for the total sleep periods. Sleep parameter
90% of B sleep/disturbed period B sleep D sleep
Remaining 10%/recovery period B sleep D sleep
Total sleep B sleep
D sleep
Stage 0 Stage 1 Stage 2 Stage 3 Stage 4 SWS REM MT TST
2.8 (0.7) 11.8 (3.8) 45.6 (4.8) 11.3 (2.0) 13.0 (3.3) 24.3 (4.6) 21.3 (5.5) 1.8 (1.0) 105.0 (8.4)
0.8 (0.4) 3.1 (1.0) 4.9 (1.8) 1.4 (1.4) 0.5 (0.5) 1.9 (1.9) 1.2 (1.2) 0.6 (0.3) 11.9 (1.1)
3.6 14.9 50.5 12.8 13.5 26.3 22.5 2.4 116.9
15.7 (5.3) * 24.8 (4.7) 93.8 (18.1) * * 8.8 (2.4) 16.3 (5.9) 25.0 (7.8) 32.7 (8.4) 3.9 (1.4) 180.2 (25.6) * *
Stage 1 latency REM latency
7.8 (2.7) * 18.3 (3.8) 59.3 (7.7) * 3.8 (1.7) ** 1.0 (0.7) * 4.8 (2.3) ** 20.2 (7.2) 2.3 (1.2) 105.0 (8.4)
4.8 (2.2) 6.5 (1.8) 34.5 (11.1) * 5.0 (1.0) 15.3 (5.9) 20.3 (6.7) * 12.5 (2.9) * 1.6 (0.6) 75.2 (18.9) * *
(1.0) (2.7) (6.0) (2.8) (3.4) (5.6) (4.7) (1.2) (9.4)
13.33 (8.9) 71.4 (6.6)
3.9 (0.7) 67.4 (10.3)
Figures represent means and standard errors (within parentheses) in minutes. Asterisks denote significant differences between baseline (B sleep) and disturbed sleep (D sleep) conditions for corresponding periods. Wilcoxon test * * < 0.03, * < 0.05, n = 6.
270
M. GILLBERG ET AI,.
FABLE II Relative power density in frequency bands during sleep stages for 90% of B sleep/disturbed period, the remaining 10%/recovery period and for the complete sleep periods. All values expressed as % of total power of baseline sleep ( = 100%). Sleep param,
Frequency band
90% of B sleep/disturbed period
Remaining 10%/recovery period
Total sleep
B sleep
D sleep
B sleep
D sleep
B sleep
St 1 +2
delta theta tot. (0.5-16 Hz)
22.5 (3.9) 7.4(1.1) 38.2 (6)
31.3 (4.4) ** 9.4(1.4) ** 50.4 (6.6) *
4.1 (l.1) 1.2(0.41 6.9 (1.9)
18.2(4.8) ** 5.0(1.3) ** 29.(I (7.6) * *
26.6 (4.l) 8.6(1.41 45.1 (6.9)
49.5 (7.1) ** 14.4(2.31 ** 79.4 (11.7~ * *
SWS
delta theta tot. (0.5 ~ 16 Hzl
33.6 (6.6) 19.5 (2.4) 41.0 (6.9)
only 2 subj. with SWS
only 1 sut~j. with SWS
27.9 (9,2) 2.(~ (0.8) 32.7 (10.6~
35.6 (7.3) 3.9 (0.4) 43,4 (7.7)
_?0,,~ (9.6~ 3.0 (0.9~ 36.3 (11 2/
REM
delta theta tot. (0.5-16 Hz)
5.6 (1.31 2.4 (0.61 10.4(2.4)
4.8 (1.4) 1.9 t0.61 8.5(2.6)
only t subj. with REM
3.5 (0.8) 1.3 (0.3) 6,1(1.41
6.3 (0.8) 2.6 (0.4) 11.5(1.5)
8.3 (1.61 3.2 (0.7) 14.6 (2.8)
All stages
delta theta tot.(0.5 16 Hz)
61.7(3.5) 13.5(l.1) 89.7(1.21
39.1 (4.7) * 11,7(1.51 62.5(6.9) **
6.7(1.21 1.610.31 10.3(1.21
49.7(11.51 ** 8.9 (1.81 ** 66.5(14.9) **
68.4(3.7) 15.1 (1.31 11141 (basel.)
D sleep
88.8 (t2,91 20.6 (2,5) * 129.0(16.51
Figures represent means and standard errors (within parentheses) in percent. Asterisks denote significant differences between baseline (B sleep) and disturbed sleep (D sleep) conditions for corresponding periods. Wilcoxon test * * < 0.03. * < 0,05: n ~ 6. Figures in italics derive from 5 subjects (1 subject lacked SWS and 1 subject lacked REM).
longer than the corresponding period during baseline sleep and contained significantly more stage 2, SWS, and REM while there were no significant differences for stages 0, 1, and MT. The disturbed sleep was significantly longer (TST; 51% _+ 12%; Wilcoxon, P < 0.03) than the baseline sleep. Also stages 0 and 2 differed significantly between the 2
conditions. Stage 1 latency and REM latency did not differ significantly, neither did the duration of the first cycle (defined as the time from onset of stage 1 to end of REM: see Table IV). Baseline sleep contained only one complete sleep cycle whereas the disturbed sleep contained at least two cycles for all subjects except one (see Table IV).
TABLE 11I Relative power density per minute in frequency bands during sleep stages for 90% of B sleep/disturbed period~ the remaining 10%/recovery period and for the total sleep periods. All values expressed as % of total power density per minute of baseline sleep ( 100%), Sleep param,
Frequency band
90% of B sleep/disturbed period
Remaining 10%/recovery period
I otal sleep
St 1 + 2
delta theta tot. (0.5 16 ttz)
B sleep
B sleep
B sleep
SWS
delta theta tot.(0.5 16 Hz)
157.7 (12.8) 19.5 (2.4) 197.2(13.51
REM
delta theta tot. (0.5-16 Hz)
All stages
delta theta tot.(0.5--16 Hz)
43.3 (5) 14.5 ( 1 . 7 1 73.8 (7.6)
D sleep 47.0(6.1) 14.1(2.11 75.4 (9.3)
D sleep
52.0(10.61 14.8 (3.7) 88.9 (17.1)
59.8(10,71 16.1 (2,5) 91.l (14.8)
only 2 subj. withSWS
only 1 subj. withSWS
/3&5 (29.21 14.0 (3.7j ~ 165.8(34. o~
27.7 (6.2) 11.5 (2.5) 51.6(11.61
32.2(4.2) 12.2(1.4) 56.0(7.11
only l subj. with REM
2&9 (6.4) 10.8 (2.5) 49.8(ll.2)
68.0 (4.0) 14.8 ( 1 . 3 1 98.7 (1.6)
43.4(5.2)** 13.1(1.71 71.5 (7.8) **
65.7(11.8) 16.0 (2.2) 101.4(10.71
81.8(15.61 ~ 15.1 (1.81 110.8(17,01 ~
45.4 (4.6) 14.7 (1.81 76,7 (7.4) 156.6 (12.6) 19.5 (2.4) 196.(1(13.5)
D sleep 46.1 (8) 13.3 (2.5) 73.5 (12.6) 15Z1 (12.4) 17.3 (2,6)* 18Q.O(lS.I)
~7.0 (4.8) i4.7 (1.31 67.5 (7.7)
33.3 (3.4) 12.5 (l 3) 57.8 (6.1)
68.4 (3.7) 15.1 (1.31 I00 (baseline)
58.6 (0.8) 13.8 (17l 86.5 (10.t)
Figures represent means and standard errors (within parentheses) in percent. * denote significant differences between baseline (B sleep) and disturbed sleep (D sleep) conditions, t denote differences between the 90% of B sleep and remaining t0% or disturbed period and recovery period. § denote differences between the recovery period of D sleep and the first 90% of B sleep. Wilcoxon test * *'tt < 0.03; .,t,§ < 0.05: n = 6. Figures in italics derive from 5 subjects (1 subject lacked SWS and 1 subject lacked REM).
271
R E C O V E R Y A F T E R SWS SUPPRESSION
The accumulated power density (Table II) was significantly reduced during the disturbed period compared to the co~responding period of the baseline sleep. The reduction was mainly in the delta band. The recovery period contained significantly more power density in all frequency bands than the corresponding period of baseline sleep. At the termination of the disturbed sleep there were no significant differences from baseline power density. The disturbed sleep contained significantly more delta, theta and total (0.5-16 Hz) power in stage 1 + 2 during both the disturbed and the recovery periods compared to the baseline sleep. Significant differences in the same direction were found also when the complete sleep periods were compared. Table III shows the intensity dimension of the power density data, i.e., relative power density per minute. Tests of significance were made for differences between conditions for the 90% of baseline/disturbed period, the remaining 10% of baseline/recovery period, and the total sleep periods, respectively, as well as between the disturbed and recovery periods and between the first 90% and the remaining 10% of baseline sleep. Also the recovery period was tested against the first 90% of the baseline sleep. The disturbed sleep was found to be slightly, but significantly, less intense in the theta band during SWS than the baseline sleep. The disturbed period was less intense than the corresponding period of the baseline sleep. The data show that it is mainly delta activity that is responsible for this difference. During the recovery period there were no significant differences
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T A B L E IV Sleep cycles: relative power density in frequency bands, durations, and n u m b e r of complete cycles.
Frequency band Delta Theta Tot. (0.5-16 Hz) Duration of cycle (min) No. of subjects with complete cycle
1st cycle B sleep
1st cycle D sleep
2nd cycle D sleep
69.7 (3.6) 15.1 (1.4) 100 (baseline)
37.0 (6.3) * * 11.8 (2.5) * 60.5 (10.7) * *
50.2 (10.8) 11.2 (2.6) 71.7 (1.4)
87.3 (10.3)
80.5 (9.0)
94.2 (6.4) 6
6
5
Relative power in percent of total power for the first cycle of baseline sleep. Asterisks denote significant differences between 1st cycle of baseline sleep (B sleep) and 1st cycle of disturbed sleep (D sleep). Wilcoxon test * * < 0.03, *0.05; n = 6. Figures in italics derive from 5 subjects.
in sleep intensity from the corresponding period of the baseline sleep. Comparing the disturbed period with the recovery period, delta intensity as well as total intensity were significantly higher during the latter. SWS theta activity was slightly less intense during the recovery period than during the first 90% of the baseline sleep. Table IV shows power density data analysed for sleep cycles. (A Friedman non-parametric ANOVA, which would have been the appropriate test, could not be used since only 5 subjects had a second cycle.) The first cycle of the disturbed sleep contained significantly less power density than that of the baseline sleep for the delta and theta bands as well as for all bands together. The duration of the first cycle did not differ between conditions.
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1
Discussion
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D/STURBED
END OF DISTURBEDSLEEP
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60
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140
RELATIVE TIME ( % of baseline ) Fig. 3. Accumulation of relative delta E E G power density for baseline and disturbed sleep over relative time. Power is expressed relative to the total amount accumulated during the baseline condition ( = 100%) and time relative to the duration of the baseline sleep (=100%). Means and standard errors, n = 6. Asterisks denote significant differences ( P < 0.05, Wilcoxon) between baseline and disturbed sleep, ns denotes non-significant differences from the baseline finishing power value, i.e., 100%. Accumulation was done by adding the means of successive 10% time intervals. The curve describing disturbed sleep is continued for as long as all subjects (n = 6) are asleep. The single symbol (open square) shows mean relative power at awakening plotted against mean relative duration for the disturbed sleep ( + 1 S.E.)
Slow wave sleep and E E G power density (especially in the delta band) were clearly suppressed by the acoustic stimulation. This effect was achieved with only slightly increased amounts of waking. Recovery was characterized by a prolongation of sleep. The increased sleep time contained mainly SWS, stage 2 and REM sleep. The results are similar to the observations of Dijk and Beersma (1989) in that suppression of delta activity led to a displacement of SWS and delta power density from their normal positions early in sleep to the latter part of sleep which had been left undisturbed. In contrast to their study, however, we obtained a very clear prolongation of sleep for the baseline condition. The reason that we were able to demonstrate this effect in our study was probably that our period of suppression
272 covered a p e r i o d c o r r e s p o n d i n g to 90% of the d u r a t i o n of the baseline sleep, leaving very little time for recovery within the n o r m a l l y expected sleep d u r a t i o n . T h u s any recovery of SWS (delta) activity would have to be a c c o m p l i s h e d via a p r o l o n g a t i o n of sleep. In the study by D i j k a n d Beersma (1989), on the other hand, the length of the suppression p e r i o d c o n s t i t u t e d only 63% a n d 50%, respectively, of the d u r a t i o n of control sleep, leaving time for c o n s i d e r a b l e recovery of the loss within the time span c o r r e s p o n d i n g to the u n d i s t u r b e d sleep condition. The rate of E E G p o w e r a c c u m u l a t i o n increased after cessation of disturbance. Since S W S contains con~idera b l y m o r e delta p o w e r d e n s i t y than other stages the increased rate of a c c u m u l a t i o n can be a t t r i b u t e d m a i n l y to the a p p e a r a n c e of SWS. (The significant differences in total delta intensity presented in T a b l e I I I can be e x p l a i n e d by the a b s e n c e of S W S d u r i n g the d i s t u r b e d p e r i o d and its presence d u r i n g the recovery period.} U n e x p e c t e d l y , there were no significant increases in delta intensity d u r i n g SWS or stage 1 + 2. If the supp r e s s i o n h a d created a " p r e s s u r e " specifically for delta activity, such an increase might have been expected. On the o t h e r hand, the level of pressure for S W S b r o u g h t a b o u t by the p r e s e n t design might, however, have been too low to stimulate an increase in S W S (delta) intensity. W h e n the s p o n t a n e o u s a w a k e n i n g occurred, the loss of S W S a n d delta p o w e r density h a d recovered completely. Stage 2 ( a n d p o w e r d e n s i t y of stage 1 + 2), however, " o v e r - r e c o v e r e d . " It increased d u r i n g recovery in spite of the fact that it had even increased signific a n t l y d u r i n g the d i s t u r b e d period. This finding argues against stage 2 a m o u n t s being i m p o r t a n t for recovery. Also R E M sleep showed a t e n d e n c y to over-recover d e s p i t e the lack of any loss during the d i s t u r b e d period. In fact, a p p r o x i m a t e l y 2 / 3 of the sleep extension consisted of stages 2 a n d R E M whereas only 1 / 3 consisted of SWS. W h a t then, was the reason for the extension of stages 2 a n d R E M ? W e suggest that the S W S deficit at the t r a n s i t i o n between the first a n d s e c o n d cycles acted as a p r o m p t to ensure a full second cycle with a n o r m a l structure, i.e., with initial stage 2 a n d a final R E M sleep period, and with the S W S p e r i o d in between. Thus, the second cycle and its c o n t e n t of stages 2 a n d R E M w o u l d be seen as the vehicle for S W S (delta) recovery. This would, again, suggest that stage 2 a n d R E M or their c o n t e n t of d e l t a activity lack h o m e o s t a t i c or recuperative value b y themselves. T h e present data, however, give only weak s u p p o r t for such an i n t e r p r e t a t i o n . S t r o n g e r evidence would have been if all stage 2 activity h a d p r e c e d e d S W S d u r i n g the recovery period. The a b o v e o b s e r v a t i o n s also attest to the r e m a r k a b l e resistance of R E M sleep. A l t h o u g h S W S was being suppressed, a R E M p e r i o d a p p e a r e d with the same
M. GILLBERG ET Air. latency a n d d u r a t i o n as that of baseline sleep. A similar resistance was o b s e r v e d b y ourselves in a recent study ( G i l l b e r g a n d A,kerstedt 1991) where we f o u n d the process of S W S (delta) recovery after total sleep loss to be i n t e r r u p t e d b y R E M sleep a n d c o n t i n u e d d u r i n g the second sleep cycle after an initial p e r i o d of stage 1 + 2 sleep. T h e latter f i n d i n g also s u p p o r t s the i n t e r p r e t a t i o n of the increased sleep d u r a t i o n in the p r e s e n t s t u d y as p a r t l y a c o n s e q u e n c e of the cyclic structure of sleep: lost S W S is m a i n l y recovered d u r i n g the regular S W S period, after the n o r m a l sequence of o t h e r stages. In conclusion, the p r e s e n t s t u d y has d e m o n s t r a t e d that s u p p r e s s i o n of S W S (delta) activity for a d u r a t i o n c o r r e s p o n d i n g to that of a n o r m a l s p o n t a n e o u s l y t e r m i n a t e d sleep will cause p r o l o n g a t i o n of sleep in o r d e r to recover the a m o u n t s lost. A direct i n t e r f e r e n c e with the S W S (delta) process starts a recovery process that is similar to that after total sleep d e p r i v a t i o n . We would like to thank G6ran Ekstr6m, GiSran Lindbeck, Karin Sigurdson and GiSran Stensson for help with data collection.
References
~,kerstedt, T. and Gillberg, M. The circadian variation of experimentally displaced sleep. Sleep, 1981, 4: 159-169. ,~kerstedt, T. and Gillberg, M. A dose-response study of sleep loss and spontaneous sleep termination. Psychophysiology, 1986a, 23: 293-297. Akerstedt, T. and Gillberg, M. Sleep duration and the power spectral density of EEG. Electroenceph. clin. Neurophysiol., 1986b, 64: 119-122. Borbdly, A.A., Bauman, t:., Brandeis, D., Strauch, 1. and Lehmann, D. Sleep deprivation: effect on sleep stages and EEG power density in man. Electroenceph. clin. Neurophysiol., 1981, 51: 483-493. Czeisler, C.A., Weitzman, E.D., Moore-Ede, M.C., Zimmerman, J.C. and Knauer, R.S. Human sleep: its duration and organization depend on its circadian phase. Science, 1980, 210: 1264-1267. Dijk, D.J. and Beersma, D.c.M. Effects of SWS deprivation on subsequent EEG power density and spontaneous sleep duration. Electroenceph. clin. Neurophysiol., 1989, 72: 312-320. Feinberg, I., March, JD.. Floyd, T.C., Jimison, R., Bossom-Demitrack, L. and Katz, P.H. Homeostatic changes during post-nap sleep maintain baseline levels of delta EEG. Electroenceph. clin. Neurophysiol., 1985, 61: 134-137. Feinberg, I.. Floyd, T.C., and March, J.D. Effects of sleep loss on delta (0.3-3 Hz) EEG and eye movement density: new observations and hypothesis. Electroenceph. clin. Neurophysiol., 1987, 67: 217--221. Gillberg, M. and ,~kerstedt, T. The dynamics of the first sleep cycle. Sleep, 1991, in press. Rechtschaffen, A. and Kales, A.A. A Manual of Standardized Terminology, Techniques, and Scoring System for Sleep Stages of Human Subjects. U.S. Government Printing Office, Washington, DC, 1968. Siegel, S. Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York, 1959. Torsvall, T., ~,kerstedt, T. and Lindbeck, G. Effects on sleep stages and EEG power density of different degrees of exercise in fit subjects. Electroenceph. clin. Neurophysiol., 1984, 57: 347-353.
RECOVERY AFTER SWS SUPPRESSION Webb, W.B. and Agnew, H.W. Stage 4 sleep: influence of time course variables. Science, 1971, 174: 1354-1356. Webb, W.B. and Agnew, H.W. The effects on subsequent sleep of an acute restriction of sleep length. Psychophysiology, 1975, 12: 367370.
273 Zulley, J., Wever, R. and Aschoff, J. The dependence of onset and duration of sleep on the circadian rhythm of rectal temperature. Pfliigers Arch. Ges. Physiol., 1981, 391: 314-318.