Eur J AppI Physiol (1994) 68:274-280 European Journal of
Applied
Physiology and Occupational Physiology © Springer-Verlag 1994
Suppression of electroencephalogram A power density during non-rapid eye movement sleep as a result of a prolonged cognitive task prior to sleep onset Masaya Takahashi, Heihachiro Arito National Institute of Industrial Health, 21-1, Nagao 6 chome, Tama-ku, Kawasaki 214 Japan Accepted: December 1, 1993
Abstract. The effects of a prolonged cognitive task prior to sleep onset on subsequent sleep patterns were examined in 14 healthy subjects who were randomly assigned to two conditions. Those assigned to a working condition were asked to engage in a prolonged cognitive task until close to bedtime (0200 hours), whereas those assigned to a relaxing condition were instructed to perform the same task during the daytime and then to stay awake in a relaxed state until the same bedtime as the work group. Visual scoring of sleep stages showed no significant differences in the amounts of stage 4 and slow wave sleep (stage 3 +4) between the two conditions. Power spectrum analysis of sleep electroencephalogram (EEG) revealed that the EEG A (0.5-4.0 Hz) power density in the first non-rapid eye movement (REM)-REM sleep cycle was significantly lower following the prolonged cognitive task prior to sleep onset than following the relaxed wakefulness and that the decreased EEG A power density in the first sleep cycle was not compensated for during the later part of the sleep. These findings would indicate that the prolonged cognitive task prior to sleep onset may suppress EEG A power density during subsequent sleep, suggesting that such a task may interfere with the development of deep non-REM sleep. Key words: Non-rapid eye movement sleep - Electroencephalogram A power density - Night work - Cognitive tasks
Introduction It has been demonstrated that shift work alters sleep quantitatively and qualitatively, and that night work in particular impairs sleep (Rutenfrantz et al. 1977; Dahlgren 1981; Torsvall et al. 1981; Rosa et al. 1989; Akerstedt 1990). In recent years, not only conventional night work but many kinds of work schedules, includCorrespondence to:
M. Takahashi
ing the shortened work week (Rosa et al. 1989), have been introduced. Because of the increasing need to work beyond normal working hours, it has been noted that work schedules extending past midnight appear to prevail in various industries, such as finance, aviation, transportation and communication (Kruger 1989). With these work schedules, workers may not sleep during the ordinary nocturnal sleep time, and their sleep may be disrupted, even if in fact they do not engage in shift work. Nevertheless, to our knowledge, little is known about the effects on sleep of prolongation of working hours prior to sleep onset. Recently, power spectrum analysis of sleep electroencephalogram (EEG) using fast Fourier transform (FFT) has been applied to studies of sleep regulation (Borb61y et al. 1981; Akerstedt and Gillberg 1986b) and shiftworkers' sleePo(Torsvall and Akerstedt 1988; Akerstedt et al. 1991; Akerstedt and Kecklund 1991). According to the two-process model of sleep regulation (Borb61y 1982; Daan et al. 1984), it has been shown that sleep is regulated by an interaction between a circadian factor referred to as process C and a homeostatic factor referred to as process S. Process S, which can be expressed as the EEG power density of the 0.5-4.0 Hz frequency range and thought of as a level of a sleep-promoting substance, has been shown to increase exponentially with increasing duration of prior wakefulness and decrease exponentially over the time-course of sleep (Dijk et al. 1987a, 1990a, b, 1991). Assuming that the two process model holds for the sleep of workers whose working hours extend prior to sleep onset, their propensity for sleep is determined both by the duration of prior wakefulness and by the circadian time of sleep onset. Work prolonged prior to sleep onset is expected to increase the EEG power density of the 0.5-4.0 Hz frequency range at the beginning of the sleep period, because of an increase in the duration of prior wakefulness. It is logical to infer on the basis of our sleep experience that the propensity for sleep is influenced not only by the duration of prior wakefulness but also by its quality, such as mental and physical activities during the pre-sleep period, depend-
275 ing o n t h e t i m e o f d a y w h e n such activities a r e p e r formed. T h e p u r p o s e o f t h e p r e s e n t s t u d y was to i n v e s t i g a t e t h e effects o f a p r o l o n g e d c o g n i t i v e t a s k p r i o r to s l e e p onset on subsequent sleep patterns, with special refere n c e to t h e t w o - p r o c e s s m o d e l o f s l e e p r e g u l a t i o n . F o r this p u r p o s e , b o t h t i m e - c o u r s e c h a n g e s in E E G p o w e r d e n s i t i e s a n d v i s u a l l y s c o r e d s l e e p stages w e r e e x a m i n e d in a g r o u p o f s u b j e c t s a s s i g n e d to t r a n s c r i b i n g E n g l i s h m a n u s c r i p t s w i t h a w o r d p r o c e s s o r p r i o r to s l e e p o n s e t , a n d c o m p a r e d with a n o t h e r g r o u p w h o d i d t h e s a m e d a y t i m e t a s k s a n d t h e n s t a y e d a w a k e in a rel a x e d s t a t e until g o i n g to s l e e p at t h e s a m e time.
IWorking
I
Time of Day 11 13 15 17 19 21 23
7
9
I
I
I
7
9
11 13 15 17 19 21
1
1
t
I
I
I
I
1 2
7
I
I I
I
23
1 2
7
I
I I
I
Adaptation Baseline Experimental IRelaxing I
I
[
I
I
I
I
Adaptation Methods
Baseline
Subjects. The subjects were 14 healthy male students [mean age 21.6 years (SD 1.7), range 20-25] who were paid to participate in the experiment. They did not report any sleep disorders. Throughout the entire experimental period, they were asked to refrain from taking beverages containing caffeine, alcohol or other drugs known to affect sleep, and not to take naps during their periods of wakefulness.
Experimental design. The subjects were randomly assigned to either a prolonged cognitive task until close to their 0200 hours bedtime (working condition) or to relaxed wakefulness until close to their 0200 hours bedtime after performing the same task during the daytime only (relaxing condition). The experimental schedule for each of these conditions is shown in Fig. 1. The working condition (n=7) consisted of 3 successive days. On the adaptation and baseline days, the subjects were asked to engage in transcribing scientific manuscripts written in English using a word processor during their working hours (1030-1800 hours) and were allowd to sleep for 8 h from 2300 to 0700 hours. The English transcription task employed in this study was considered to be cognitively very demanding, because most Japanese students are not used to such a task. During their working hours, the subjects were allowed to complete their tasks at their own pace, and neither punishment nor reward was given for their results. On the experimental day, working hours were prolonged to 1 h before the 0200 hours bedtime. The subjects were allowed to sleep during the 5-h period from 0200 to 0700 hours and awakened by the experimenter at 0700 hours. The relaxing condition (n=7) also consisted of 3 successive days. The same schedule as that of the working condition was applied to the adaptation and baseline days. On the experimental day, the subjects were asked to finish transcribing the manuscripts at 1800 hours and stay awake in a relaxed state until 0200 hours. Then they were allowed to sleep during the 5-h period from 0200 to 0700 hours and were awakened at 0700 hours by the experimenter. During the relaxing periods in the entire experiment, the subjects remained in the rest room and relaxed (watching television, listening to music, and reading books) together with the experimenter. Data recording and analys&. The EEG, electro-oculogram (EOG) and submental electromyogram (EMG) were recorded throughout the night. Sleep EEG were derived from C3-A1 and C4-A2. Electrocardiogram (ECG) was also continuously recorded throughout the entire experimental period. All signals were recorded with an ambulatory EEG recorder (Medilog-9000, Oxford Medical Limited, UK). The recorded EEG, EOG and EMG were transcribed on to paper at a speed of 10 m m . s - I using an electroencephalograph (Type 1A59, NEC San-ei, Japan). The time constant of the E E G and EOG signals was set at 0.3 s. Sleep stages were visually
Experimental lwork
[-]Relaxing ~ M e a l
~Sleep
Fig. 1. Experimental schedules for working and relaxing conditions. Each set of conditions consisted of 3 successive days, i.e. adaptation, baseline and experimental days. For details, see Methods
scored for 30-s epoch according to the criteria of Rechtschaffen and Kales (1968). The sleep EEG (C3-A1) was subjected to power spectrum analysis with an FFT routine on a microcomputer (Signal Processor 7T18, NEC San-ei, Japan). The sleep EEG signal was filtered (high cut filter: 30 Hz) and sampled at a frequency of 64 Hz, yielding analysis intervals of 8.0 s (512 points). The average power spectrum was calculated over three successive 8-s power spectra, resulting in one spectrum every 30-s epoch. The integrated EEG power density of the time-averaged power spectrum was computed across the A (0.5M.0 Hz) frequency range. Epochs contaminated by artefacts were excluded by visual inspection of the polygraphic record. Since the interindividual differences in the absolute values of the integrated EEG power density were quite large, the integrated EEG power density of the A frequency range was standardized in accordance with the method of Dijk et aI. (1990a). Accordingly, the integrated EEG power density of the A frequency range was time-averaged in each non-rapid eye movement (nREM) sleep period (including stage 1) per nREM-REM sleep cycle. Then, the average A power density per nREM-REM sleep cycle was expressed as a percentage of the mean A power density in all nREM sleep periods during the baseline night. The nREMREM sleep cycles were defined according to the criteria of Feinberg and Floyd (1979) as the succession of a nREM sleep period (including stage 1) of at least 15-min duration and a REM sleep period of at least 5-min duration; no minimal REM sleep duration was required for the first and last nREM-REM sleep cycle.
Statistical analysis. The sleep variables derived from the visual scoring of sleep stages and the EEG A power density by FFT were submitted to a two-way analysis of variance (ANOVA) with repeated measures, with the factors of sleep-shortening (baseline, experimental nights) and late-night working (working, relaxing conditions).
276
the working condition (a) and the relaxing condition (b). Under the working condition, the level of EEG A power density in the first nREM-REM sleep cycle was lower during the experimental night than during the baseline night. On the other hand, it tended to be enhanced under the relaxing condition in comparison with the baseline night. Figure 3 shows the changes in average A power density per nREM-REM sleep cycle on baseline and experimental nights under the working condition and the relaxing condition. The ANOVA revealed that in the first sleep cycle, there was a statistically significant main effect of the late-night working for the average A power density (F(1,24)=4.91, P<0.05), showing that the power density was significantly decreased in the first sleep cycle of the working condition as compared with that of the relaxing condition. There was not a statistically significant interaction effect between the sleep-shortening and the late-night working. The A N O V A also revealed that there were no statistically significant main effects of the sleep-shortening or the late-night working, as well as significant interaction effects between these two fators for the average A power density in the second and third sleep cycles.
Results
Visually scored sleep variables Table 1 gives the sleep variables on baseline and experimental nights under both working and relaxing conditions. The two-way ANOVA showed statistically significant main effects of the sleep-shortening for the amounts of stage 1 (F(1,24)=26.39, P<0.01), stage 2 (F(1,24) = 60.45, P < 0.01), and REM sleep (F(1,24) =71.86, P<0.01) for the entire sleep period. There were no statistically significant interaction effects between the sleep-shortening and the late-night working for these sleep variables. For each nREMREM sleep cycle, the A N O V A revealed that in the first and second sleep cycles, there were no statistically significant main effects of the sleep-shortening or the late-night working, as well as significant interaction effects between these two factors for the sleep variables. In the third sleep cycle, there was a statistically significant main effect of the sleep-shortening for the cycle duration (F(1,23)= 5.11 P < 0.05), without a significant interaction effect between the factors.
EEG power density Discussion
Figure 2 depicts typical examples of the time courses of the visually scored sleep stages and the EEG A power density during baseline and experimental nights under
Working condition W1
In the present study, a group of subjects was asked to perform an English transcription task, which was cog-
Relaxing condition Baseline Experimental
b
Baseline
,i' i |,!
III II ~ '12 % C ~6 O
<3 (.9 LIJ
23
72
7 23 Time of Day
Fig. 2. Typical examples of the time course of electroencephalogram A (0.5-4.0 Hz) power density and visually scored sleep stages on baseline and experimental nights under working condi-
7 2
7
tion (a) and relaxing condition (b). All data were plotted for 30 sec epoch. W, Wakefulness; R, rapid eye movement sleep; $1-$4, stage 1 to stage 4 sleep
277 Table 1. Sleep variables for the entire sleep period and each non-rapid eye movement-rapid eye movement (nREM-REM) sleep cycle on baseline (B) and experimental (E) nights under both working (W) and relaxing (R) conditions W (n =7)
R (n=7)
B
E
2-Way ANOVA
B
E
Main effects
Interaction
mean
SEM
mean
SEM
mean
SEM
mean
SEM
W/R
B/E
Entire sleep period Total sleep time (min) Sleep latency (min) REM latency (min) Wakefulness (min) Stage 1 (min) Stage 2 (min) Stage 3 (rain) Stage 4 (min) SWS (stage 3 +4, min) REM sleep (min)
461.2 7.2 85.8 18.7 39.9 186.1 53.6 75.4 129.0 106.1
11.4 1.7 7.9 11.3 2.4 13.9 11.6 13.5 18.3 5.3
294.4 4.7 78.8 5.6 20.6 104.9 33.5 70.9 104.4 64.5
2.4 2.1 10.1 2.4 2.5 5.6 6.2 6.4 5.4 5.6
468.6 9.2 64.9 11.0 47.1 206.2 40.8 48.5 89.3 126.0
2.8 2.9 5.5 2.8 5.6 13.7 7.0 12.2 16.8 6.7
292.2 7.2 76.6 7.9 27.7 107.7 28.6 61.1 89.8 67.1
2.9 3.0 5.6 2.9 3.7 11.0 3.4 13.6 11.5 6.0
NS NS NS NS NS NS NS NS NS NS
0.01 NS NS NS 0.01 0.01 NS NS NS 0.01
NS NS NS NS NS NS NS NS NS NS
Cycle 1 n Cycle duration (rain) REM latency (min) Wakefulness (rain) Stage 1 (rain) Stage 2 (rain) Stage 3 (min) Stage 4 (rain) SWS (stage 3+4, rain) REM sleep (rain)
7 104.5 85.8 0.2 9.7 20.9 13.4 42.6 56.1 17.9
10.9 7.9 0.2 3.0 7.3 2.5 6.3 4.9 3.8
7 104.3 78.8 0.5 7.2 21.2 12.0 41.7 53.7 21.7
14.0 10.1 0.5 2.1 5.7 3.4 6.7 7.3 3.9
7 80.8 64.8 0.0 6.3 20.9 12.1 26.7 38.9 14.7
7.0 5.5 0.0 1.3 4.2 1.6 6.0 5.2 2.7
7 94.0 76.6 0.2 6.1 18.0 13.7 39.6 53.3 16.6
5.1 5.6 0.1 2.0 3.8 1.7 8.7 7.5 2.6
NS NS NS NS NS NS NS NS NS
NS NS NS NS NS NS NS NS NS
NS NS NS NS NS NS NS NS NS
Cycle 2 n Cycle duration (rain) REM latency (min) Wakefulness (rain) Stage 1 (min) Stage 2 (rain) Stage 3 (rain) Stage 4 (rain) SWS (stage 3+4, min) REM sleep (rain)
7 112.8 79.6 0.0 6.1 40.1 20.3 16.1 36.4 30.1
10.0 4.7 0.0 2.1 4.1 5.4 4.8 8.1 5.4
7 101.1 73.5 0.1 4.9 36.8 12.6 21.3 33.9 25.6
4.4 4.1 0.1 1.5 4.4 2.9 5.2 5.9 3.6
7 109.8 72.6 0.0 6.9 42.0 13.8 14.0 27.8 33.1
9.0 4.2 0.0 1.8 6.3 3.8 5.2 3.1 6.4
7 104.3 68.8 0.4 10.2 41.4 9.8 12.6 22.4 29.9
5.3 3.7 0.4 1.8 5.4 3.0 4.7 5.7 3.5
NS NS NS NS NS NS NS NS NS
NS NS NS NS NS NS NS NS NS
NS NS NS NS NS NS NS NS NS
Cycle 3 n Cycle duration (rain) REM latency (rain) Wakefulness (min) Stage 1 (min) Stage 2 (rain) Stage 3 (min) Stage 4 (rain) SWS (stage 3+4, min) REM sleep (min)
7 109.8 80.7 0.6 7.6 53.6 13.3 9.7 23.0 24.9
11.8 8.3 0.4 1.1 5.9 4.9 4.6 7.2 5.9
6 83.3 60.0 0.0 7.5 40.5 8.6 6.6 15.2 20.1
12.3 6.9 0.0 1.7 6.7 3.3 2.6 5.2 6.4
7 99.8 65.7 0.1 9.3 49.6 8.3 2.0 10.3 30.6
5.1 5.2 0.1 1.7 4.3 4.0 1.8 5.5 6.6
7 85.4 60.8 0.0 8.2 42.5 5.1 8.9 14.1 20.6
4.6 6.0 0.0 1.6 7.6 2.3 7.1 8.0 4.6
NS NS NS NS NS NS NS NS NS
0.05 NS NS NS NS NS NS NS NS
NS NS NS NS NS NS NS NS NS
n i t i v e l y v e r y d e m a n d i n g at l e a s t f o r J a p a n e s e s t u d e n t s , until c l o s e to 0200 h o u r s b e d t i m e , w h i l e a n o t h e r g r o u p was a s k e d to d o t h e s a m e t a s k until 1800 h o u r s a n d t h e n stay a w a k e r e l a x i n g u n t i l t h e s a m e b e d t i m e . A sign i f i c a n t d e c r e a s e in t h e E E G A p o w e r d e n s i t y in t h e first n R E M - R E M s l e e p cycle w i t h o u t a n y c h a n g e s in visually scored slow wave sleep (SWS) under the working c o n d i t i o n w o u l d i n d i c a t e t h a t t h e p r o l o n g e d cognitive t a s k p r i o r to s l e e p o n s e t h a d a s u p p r e s s i v e effect o f t h e E E G A p o w e r density. This E E G r e s p o n s e was in contrast with that predicted by the two-process model
o f s l e e p r e g u l a t i o n (Borb61y 1982; D a a n et al. 1984). A c c o r d i n g to this m o d e l , t h e l e v e l o f t h e p r o c e s s S, m e a s u r e d b y E E G 2~ p o w e r d e n s i t y , is s u p p o s e d l y d e termined only by the duration of prior wakefulness. T h e p r e s e n t finding, h o w e v e r , c a n b e t a k e n to i n d i c a t e t h a t in a d d i t i o n to t h e f a c t o r o f t h e d u r a t i o n o f p r i o r w a k e f u l n e s s , p r o c e s s S was also a f f e c t e d b y t h e q u a l i t y o f p r i o r w a k e f u l n e s s , such as t h e d e m a n d i n g c o g n i t i v e t a s k p r i o r to s l e e p onset. A l t h o u g h it has b e e n d e m o n s t r a t e d t h a t p o w e r s p e c t r u m analysis of s l e e p E E G b y FFT provides more quantitative and precise descrip-
278 Table 1 (continued) R (n = 7)
w (n = 7)
2-Way ANOVA
E
B
mean
SEM
6 86.7 52.4 0.0 8.8 39.8 3.1 2.4 5.5 32.6 3 86.6 72.2 1.8 7.3 64.0 1.2 0.0 1.2 12.3
mean
E SEM
mean
SEM
7.9 7.2 0.0 1.8 6.3 1.9 2.2 3.3 6.2
7 103.6 68.9 0.1 11.3 52.2 4.1 5.8 9.9 30.2
8.3 5.8 0.1 2.2 5.3 1.7 5.1 6.6 5.2
10.2 6.5 1.8 0.4 7.1 0.6 0.0 0.6 1.9
5 70.8 48.2 0.1 11.4 35.8 2.8 0.0 2.8 20.8
5.3 3.8 0.1 2.0 2.8 1.7 0.0 1.7 7.3
mean
Main effects SEM
W/R
Interaction
B/E
Cycle 4 n
Cycle duration (min) REM latency (min) Wakefulness (min) Stage 1 (min) Stage 2 (min) Stage 3 (min) Stage 4 (min) SWS (stage 3 + 4, rain) REM sleep (min) Cycle 5 n
Cycle duration (rain) REM latency (min) Wakefulness (min) Stage 1 (rain) Stage 2 (min) Stage 3 (min) Stage 4 (rain) SWS (stage 3 + 4, rain) REM sleep (min) SWS, Slow wave sleep
220
180
"a 1 4 0
0
uJ I.U
100
B
E
60
3
4
nREM-REM cycle
Fig. 3. Average A power density in non-rapid eye movement (nREM) sleep per n R E M - R E M sleep cycle on baseline and experimental nights under the working condition and the relaxing condition. Mean and standard error. For each subject, average A power density was calculated for individual n R E M sleep periods and expressed as a percentage of the mean 2xpower density in all n R E M sleep periods during the baseline (B) night. From cycle 1 to 3, values on the left side are on B nights, and those on the right side are on the experimental nights (E). For cycles 4 and 5, only values on the B nights are plotted. • Working; O relaxing
tions of changes in deep n R E M E E G signals in response to manipulated duration of prior wakefulness as compared with visual scoring (Borbdly et al. 1981; Borbdly 1982; Daan et al. 1984; Akerstedt and Gillberg 1986b; Brunet et al. 1988; Dijk et al. 1987a, 1990a, b,
1991), the present finding suggests that the E E G A power density also reflects changes in the manipulated quality of prior wakefulness more sensitively than does the visually scored SWS. Suppression of SWS by acoustic stimulation has been reported to induce a compensatory increase in the E E G A power density during the later undisturbed part of the sleep period (Dijk et al. 1987b; Dijk and Beersma 1989; Gillberg et al. 1991). It may be speculated from these reported findings that the E E G A power density in the first n R E M - R E M sleep cycle suppressed by the prolonged cognitive task is homeostatically compensated for during the later sleep period. It is noteworthy in the present study that the prolonged cognitive tasks prior to sleep onset did not induce a rebound increase in E E G zX power density during the second and third n R E M - R E M sleep cycles. The absence of the rebound increase in the E E G 2x power density in the second and third n R E M - R E M sleep cycles may be interpreted as showing that the suppressive effect of the prolonged cognitive task on the E E G A power density may continue beyond the first n R E M R E M sleep cycle. On the basis of reported findings on a reciprocal interaction between n R E M sleep intensity and R E M sleep pressure (Beersma et al. 1990; Brunner et al. 1990) and on modifications of R E M sleep following some cognitive tasks (Mandai et al. 1989; Smith and Lapp 1991), it may be speculated that the suppression of the E E G A power density by the prolonged cognitive tasks prior to sleep onset may be due to a second-
279 ary effect of the task-induced R E M sleep alterations, particularly an increased R E M sleep pressure. H o w e v er, no such increased R E M sleep pressure was found in the present study; there were no significant differences in the a m o u n t of R E M sleep or R E M sleep latency for the first, second or third sleep cycles b e t w e e n baseline and experimental nights or b e t w e e n the working and relaxing conditions (Table 1). Thus, the present findings m a y imply that the prolonged cognitive tasks prior to sleep onset have an affect primarily on deep n R E M sleep rather than R E M sleep. It m a y also be interpreted as showing that R E M sleep is m o r e resistant to changes in the length and quality of prior wakefulness than n R E M sleep, in view of several reports which have d e m o n s t r a t e d that both R E M sleep and b o d y t e m p e r a t u r e are m o r e closely coupled to an endogenous circadian clock than n R E M sleep (Czeisler et al. 1980; A k e r s t e d t and Gillberg 1981, 1986a; E n d o et al. 1981; Dijk et al. 1990a, 1991; Gillberg and A k e r s t e d t 1991). With regard to the functional significance of the E E G A p o w e r density, t e m p o r a l relationships b e t w e e n this E E G p a r a m e t e r and endocrinological and i m m u nological processes have b e e n reported: a certain level of E E G A p o w e r density appears to be required as a trigger to facilitate growth h o r m o n e secretion (Takahashi 1979; A s t r 6 m and J o c h u m s e n 1989). T h e onset of visually scored SWS in the first n R E M - R E M sleep cycle has b e e n temporally related to an abrupt increase in the plasma interleukin-1 activity (Moldofsky et al. 1986). F r o m these lines of evidence, it would s e e m likely that a prolonged cognitive task prior to sleep onset m a y adversely affect such endocrinological and immunological processes m e d i a t e d through the suppression of the E E G A p o w e r densiy or deep n R E M sleep. In conclusion, a prolonged cognitive task prior to sleep onset m a y induce suppression of the E E G A p o w e r density during subsequent sleep, suggesting that such a task m a y interfere with the d e v e l o p m e n t of deep n R E M sleep.
Acknowledgements. The authors are deeply grateful to Dr. Roger R. Rosa, National Institute for Occupational Safety and Health, United States of America for critically reviewing the manuscript.
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