Fundamental Research. Dynamics ofEEG Slow-Wave Activity and Core Body. Temperature in Human Sleep After. Exposure to Bright Light. Christian Cajochen ...
Sleep. 15(4):337-343 © 1992 American Sleep Disorders Association and Sleep Research Society
Fundamental Research Dynamics ofEEG Slow-Wave Activity and Core Body Temperature in Human Sleep After Exposure to Bright Light Christian Cajochen, *Derk-Jan Dijk and Alexander A. BorbeIy Institute of Pharmacology, University of Zurich, Zurich. Switzerland
Summary: In seven subjects sleep was recorded after a single 3-hour (2100-0000 hours) exposure to either bright light (BL, approx. 2,500 lux) or dim light (DL, approx. 6 lux) in a crossover design. The latency to sleep onset was increased after BL. Whereas rectal temperature before sleep onset and during the first 4 hours of sleep was higher after BL than after DL, the time course of electroencephalographic (EEG) slow-wave activity (SWA, EEG power density in the range of 0.75-4.5 Hz) in nonrapid eye movement sleep (NREMS) differed only slightly between the conditions. After BL, SWA tended to be lower than after DL in the first NREMS-REMS cycle and was higher in the fourth cycle at the time when the rectal temperature did not differ. The differences in SWA may have been due to a minor sleep-disturbing aftereffect of BL, which was followed by a rebound. The data are not in support of a close relationship between SWA and core body temperature. Key Words: Core body temperature-Light-Slowwave sleep-Slow-wave activity-Spectral analysis-Sleep homeostasis.
Until the early eighties it was assumed that light exposure does not affect the human circadian system (1). Lewy et al. (2) were the first to demonstrate that bright light (BL) (approx. 2,500 lux) suppresses the plasma melatonin level in humans. Subsequently, it was shown that the circadian rhythms of core body temperature, cortisol, urine output and alertness exhibit phase shifts after scheduled exposure to BL (3-5). For example, the rhythms of both body temperature and cortisol were phase delayed after repeated exposure to BL in the evening (4), whereas a repeated exposure to BL in the early morning resulted in an advance in the rise of body temperature (6). When the sleep-wake cycle was held constant, BL exposure in the morning advanced the circadian rhythms of melatonin and body temperature and shortened rapid eye movement sleep (REMS) latency, whereas BL exposure in the evening delayed these Accepted for publication March 1992. Address correspondence and reprint requests to A. A. BorbeIy, Institute of Pharmacology, University of Zurich, Gloriastr. 32, 8006 Zurich, Switzerland. *Present address: Center for Circadian and Sleep Disorders Medicine, Harvard Medical School, Brigham and Women's Hospital, Boston, MA 02115, U.S.A.
rhythms (7). Taken together, the results indicate that light affects the phase of a single circadian pacemaker. Also, the findings could contribute to the understanding of light therapy for disorders in which a circadian pathophysiology is thought to be prevalent [e.g. certain sleep disorders (8), jet lag (9), shift work difficulties (10) and seasonal affective disorder (SAD) (11)]. The effects of BL exposure on sleep parameters and the sleep electroencephalogram (EEG) are not yet well documented. In most studies with repeated BL exposure in the morning or in the evening, only selected sleep parameters (e.g. sleep onset time, REMS latency and total sleep time) were analyzed (12,13). Light scheduled in the morning reduced sleep duration at the expense of REMS, whereas the EEG power density (in the range of 0.25-15 Hz) was not affected (6,14). Effects of light on body temperature have been recently documented. Thus, Badia et al. (15) reported that a single exposure to BL in the evening caused an immediate elevation of tympanic temperature. We confirmed that a single 3-hour exposure to BL in the evening elevates core body temperature (16). This manipulation had an immediate effect that persisted for the first 4 hours of the subsequent sleep episode. Whereas the elevated rectal temperature was
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C. CAJOCHEN ET AL.
accompanied by an increase in sleep latency, no significant effect on the visually scored sleep stages was found. This finding was surprising as manipulations of body temperature both prior to sleep and during sleep have been shown to increase slow-wave sleep (SWS) (17-19). Also other authors have proposed a close n~ lationship between SWS and temperature regulation (20,21). To examine the repercussions oflight-induced temperature changes on sleep regulation, we analyzed the dynamics ofEEG slow-wave activity (SW A; EEG power density in the 0.75-4.5-Hz band), an indicator of sleep homeostasis, and its relation to core body temperature. METHODS Subjects and design The experiment was carried out in February and March at the Institute of Pharmacology, University tDf Zurich. Eight male subjects (age range 23-32 years) were selected. All had regular sleep habits and were free of sleep complaints. The selection of subjects was based on a questionnaire in which the sleep habits, the medical history and the use of caffeine, alcohol and other drugs were assessed. Subjects with sleep complaints, a significant medical history or drug use were excluded from the study. The data of one subject could not be used for analysis for technical reasons. The experiment took place on three consecutive days. A first night in the sleep laboratory served for adaptation. On the evenings of the second and third day, subjects reported at 1930 hours to the laboratory where the EEG, electromyogram (EMG) and electrooculogram (EOG) electrodes were attached, and a rectal probe was provided. From 2100 to 0000 hours they were exposed to either BL (approx. 2,500 lux measured at eye level) or dim light (DL, approx. 6 lux) in a crossover design (three subjects were first exposed to BL; four first to DL). During the BL, subjects sat at a desk in front of a light screen (65 x 120 cm) consisting of eight white fluorescent tubes (Luxsana, true light with UV A and B, Duro-Test). The lower edge of the light screen was situated 80 cm above the floor. The distance between the subjects and the light source was not more than 1.5 m. They were allowed to read, play games or listen to music from a local radio station and were under continuous surveillance to prevent sleep. During the exposure period and the subsequent skep period, rectal temperature was recorded continuously. Every 30 minutes (between 2115 and 2345 hours) a 3-minute period was scheduled for recording the waking EEG. The subjects were requested to close their eyes for 1 minute and then to fixate a point on the wall for 2 minutes. After the 3-hour light exposure period Sleep, Vol. 15, No.4, 1992
the subjects went to bed at 0000 hour in a completely darkened and sound-attenuated room in the sleep laboratory. Polygraphic sleep recordings were obtained. Bed rest was terminated at 0745 hours. EEG recording and analysis EEG, EOG and submental EMG were recorded on paper (paper speed of 10 mm/second) with a Grass 78-D polygraph. The amplitude frequency of the highpass filters for the EEG was set to 0.1 Hz, which corresponds to a time constant of 0.6 second. EEGs were derived from C3-A2 and C4-Al, but only one derivation (usually C3-A2) was used for the analysis. All signals were recorded with gold disc electrodes (Grass Instruments type E5GH), filled with electrode cream (EC2 Grass) and fixed with collodium. The data were stored on analog magnetic tape (Hewlett Packard 3968A). In addition, two EEGs, one EMG and one EOG were on-line digitized (sampling rate: 128 Hz) by a signal processor board (containing a TMS-32010 chip of Texas Instruments) of a personal computer (PC; Olivetti-M24). Before digitizing, the EEG was low-pass filtered at 25 Hz (24 dB/octave) and on-line processed by a Radix 8 FFT routine, which was implemented on the signal processor board. The spectra were computed with a rectangular window for 4-second epochs. To obtain a mean spectrum per 20 seconds, five 4-second spectra were averaged off-line. Four-second epochs, during which the limit of the AD converter was reached (usually due to artifacts caused by movements), were excluded. Further data reduction was achieved by collapsing values into 0.5-Hz (in the range of 0.25-5.0 Hz) or I-Hz (5.25-25.0 Hz) bins. All EEG recordings were visually scored for 20-second epochs according to the criteria of Rechtschaffen and Kales (22). A time signal generated by the PC every 20 seconds allowed an accurate sychronization between power spectra and visual scores. The sleep scores were also stored in the pc. Rectal temperature recording Rectal temperature was continuously recorded during the exposure period and bed period. The temperature values were digitized and stored every 8 seconds by a portable temperature sampler (Minilog TA, V2). The temperature probe (diameter 5 mm, resolution 0.02°C) was inserted approximately 10 cm into the rectum. Statistics For statistical analyses (ANOV A, two-tailed t test) the SAS statistical package (SAS software, SAS Institute Inc., Cary, NC, U.S.A) was used.
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LIGHT EFFECTS ON SLEEP EEG AND TEMPERATURE TABLE 1. Sleep stages per NREMS-REMS cycle for the dim light (DL) and bright light (BL) conditiona
Stage
Cycle
Condition
W
2
I
DL BL
0.2 0.1
0.1 0.1
0.5 0.2
0.2 0.1
1.9 1.2
0.6 0.5
6.6 0.8
2.9 0.2
12.0 4.0
3.5 0.8
DL BL
0.7 0.7
5.7 4.9
1.4 1.6
7.8 8.2
2.0 1.6
1.2 1.5
36.8 36.2
5.1 2.1
51.7 47.1
5.2 6.1
41.5 33.5 179.3 175.6
5.5 3.8
4.1 2.3
11.5 8.9 40.6 39.1 2.3 5.6
2
DL BL
1.8 1.9 21.6 19.3
3
DL BL
13.6 11.8
1.9 2.0
9.6 10.6
1.6 1.8
8.0 11.5
4
DL BL DL BL
33.1 28.1
5.0 8.1
16.0 18.7
5.4 6.0
1.8 4.9
46.7 39.9
4.7 9.2
25.5 29.3
5.1 5.3
9.8 16.4
1.8 1.7 0.7 1.9 2.2 2.8
REMS
DL BL
14.5 13.3
6.4 2.5
24.1 27.8
3.2 5.6
19.7 36.5
MT
DL BL
0.8 0.7
0.2 0.2
2.3 1.2
0.4 0.3
1.8 1.9
SWS
Total sleep episode
4
3
1.1 3.3
4.5 4.5 1.4 2.3 1.1
3.4 9.0
1.6 2.5 3.8
5.5 4.3
31.7 22.1
6.8 b 3.9 b
0.5 0.4
2.6 2.1
0.6 0.5
36.2 40.5
8.6 8.9 2.9 4.4
53.5 55.0
8.3 11.5
89.8 95.5
6.7 12.4
111.4 111.6
9.4 7.5
9.4 7.8
1.3 12.1 11.2
1.2
REMSL
DL BL
58.6 49.4
SL
DL BL
9.9 29.7
1.5' 12.6 c
TST
DL BL
422.0 416.2
7.5 13.3
49.4 DL 395.7 409.1 58.6 BL u Mean values (minutes) SEM (n = 7); W, waking; MT, movement time; SWS, stages 3 + 4; REMSL, REM sleep latency; SL, sleep latency; TST, total sleep time; SWA, slow-wave activity (0.75-4.5 Hz) in NREMS (/LV2). h REMS episode 4 not completed in all subjects (see Methods). ,. Significant differences between DL and BL (p < 0.05; paired t test). SWA
RESULTS Sleep stages Table 1 indicates the sleep stages for the four nonrapid eye movement sleep (NREMS)-REMS cycles and for the total sleep episode. The cycles were defined according to the criteria of Feinberg and Floyd (23), with two exceptions: for cycle 4, a minimum of 5-minute REMS following NREMS was required, and for cycle 2-4 the first 20-second interval after REMS was taken as the starting epoch of the cycle. The latency to sleep onset (i.e. the interval from lights off to the first occurrence of stage 2 or REMS) was significantly longer after the exposure to BL (BL: 29.7 ± 12.6; DL: 9.9 ± 1.5 minutes ± SEM; p < 0.05 paired t test on log-transformed values; the data were log transformed because the original data were not normally distributed), whereas the latency to REMS (i.e. the interval between sleep onset and the first occurrence of REM sleep) was slightly shorter but not significantly different from DL (BL: 49.4 ± 11.2; DL: 58.6 ± 12.1 minutes; p > 0.05). The midpoints of corresponding NREMSREMS cycles did not differ significantly between the conditions.
Over the entire sleep episode, none of the sleep stages differed significantly between the conditions (p > 0.05; paired t test). The time course of SWS and REMS was analyzed with a two-factor ANOYA for repeated measures on both factors (cycle: 1-4; condition: DL, BL). For this analysis SWS and REMS were expressed as a percentage of total sleep time per NREMS-REMS cycle. The effect of cycle was significant for both SWS (F3 ,I8 = 52.83; P < 0.001) and REMS (F2 • I8 = 5.31; P < 0.05). However, neither for SWS (F I •6 = 0.35) nor for REMS (F I ,6 = 5.90) was a significant effect of condition observed (SWS: p > 0.2; REMS: p = 0.051). No significant interaction between the factors condition and cycle was present (SWS, F 3,I8 = 0.71; P > 0.5; REMS, F2• I8 = 1.10; p > 0.1). Time course of EEG power density Because only four cycles were completed by all subjects, the analysis was limited to these cycles. The upper two panels of Fig. 1 illustrate the changes of EEG power density in NREMS for the BL and DL condition. As previously (24), the mean power density iIi NREMS was expressed for each of the cycles 2-4 relative to Sleep, Vol. 15, No.4, 1992
1C. CAJOCHEN ET AL.
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For a more detailed visualization of the time course ofSWA and rectal temperature, each NREMS episode was subdivided into 20 5-percentiles, and each REMS episode into 4 25-percentiles regardless of the absolute NREMS-eplsodes episode duration (25). Mean values for SWA and rectal (BUDl) temperature were computed for each of these percentiles (Fig. 2). SWA exhibited a buildup in the first part ofNREMS episodes and a rapid decline prior to the REMS episodes. Also, the typical declining trend of SWA over successive NREMS episodes was present (26). Although the first three REMS episodes in the BL condition showed an earlier onset than in the DL condition, the differences were not significant. Rectal temperature in DL was significantly lower than in BL during the last hour of the exposure time (Table 2) and in the first 4 hours of sleep (16). In the second part of sleep the differences became progressively smaller. For a statistical analysis of the change of SWA over cycles and its buildup within NREMS episodes, mean SWAin NREMS (SW Amean) and SWA averaged over the first 30 minutes of an NREMS episode (NREMSSWA30 min) were computed for each cycle. A repeatedmeasure ANOV A for each SWA parameter with fac10 15 20 25' tors time and condition revealed a significant effect of time and condition (p < 0.05, for both SWA paramFrequency (Hz) eters). Posthoc comparisons of BL and DL showed
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FIG. 1. Change of power density during NREMS over consecutive NREMS-REMS cycles after exposure to BL and DL (upper two panels). For each frequency bin, subject and condition spectral values are expressed'relative to the value in the first NREMS-REMS cycle (=100%). Geometric means are plotted. Lines above the abscissa ipdicate frequencies for which a one-way ANOV A on the log-transformed spectral values reveal a significant effect of cycle (p < 0.05). In the lower two panels spectral values of BL are expressed relative Sleep, Vol. 15, No.4, -1992
cycle 1. In both experimental conditions power density decreased from cycle 1 to 4, particularly in the delta and theta frequencies. The largest reduction was present in the 1.5-2.0-Hz band. In the third panel of Fig. 1 the BL values are expressed relative to the corresponding DL values. In cycle 1 power density in the 0.75-1.00-Hz band was significantly lower in BL than in DL, whereas in cycle 4 the opposite changes were seen for the 0.25-2.00-Hz band. Significantly lower values in BL were observed also in the 15.25-17.00-Hz band in cycle 3 and in the 16.25-18.00-Hz and 22.25-23.00-Hz bands in cycle 4. In REMS, significant reductions in BL occurred only in the first cycle (4.75-5.00 Hz; 15.25-18.00 Hz; 24.2525.00 Hz; data not shown). Over the entire sleep episode no significant changes were seen in the spectra ofNREMS and REMS (bottom panel Fig. 1).
to the average value ofDL (=100%). Lines above the abscissa indicate frequency bins in which a significant difference between corresponding cycles (1-4) was present (paired t test on log-transformed . data; p < 0.05).
341
LIGHT EFFECTS ON SLEEP EEG AND TEMPERATURE
TABLE 2. Rectal temperature during dim light (DL) and bright light (BL) exposure prior to sleepa
-u 0
-
Time of day
36.25
36.67 (0.15) 36.61 (0.14) 36.54 (0.13) 36.48 (0.13) 36.44 (0.12)* 36.40 (0.13)*
36.62 (0.13) 21.00-21.30 36.51 (0.12) 21.30-22.00 36.41 (0.13) 22.00-22.30 36.32 (0.16) 22.30-23.00 36.19 (0.16) 23.00-23.30 36.04 (0.15) 23.30-24.00 a Mean values ("C) SEM per 30 minutes (n = 7). Significant differences between DL and BL indicated by *p < 0.01 (paired t test).
....Q)::J
ro .... 36.00 ~
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(ij
BL
DL
35.75
0
Q)
a:
condition (F1.6 = 0.41; p > 0.05) and no significant interaction (F3 18 = 0.36; P > 0.05). The mean r~ctal temperature per cycle (TEMP~ean) was higher in the first three cycles after BL than after DL (p < 0.01). The change of rectal temperature in the first 30 minutes of a NREMS episode was determined by computing the difference between the mean 5-minute value preceding the episode and the mean value of the 2530-minute interval. There were no significant differences between BL and DL.
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200
EEG power density in the waking EEG
• 1.5
3 Hours
4.5
6
FIG. 2. Dynamics of SWA and rectal temperature for BL (interrupted lines) and DL (continuous lines). Hatched areas indicate ± I SE. Mean percentiles (n = 7); SWA is expressed as the percentage of the mean NREMS value (100%). The bars above the abscissa indicate REMS episodes (REMS episode 4 is incomplete; open bars = BL; filled bars·= DL). The curves connect mean values for percentiles and are plotted relative to the mean onset and termination 9f each cycle (see text).
The analysis of the waking EEG was limited to artifact-free epochs (59.5% of all epochs; artifacts were frequent due to movements and eye blinks). The EEG power density in the 3.75-8.00-Hz range showed a trend toward lower values in the BL condition (eyes open) compared to DL (p < 0.1; data not shown). However, neither for the eyes open nor for the eyes closed condition were there any significant differences between BL and DL. DISCUSSION
Exposure to BL in the evening increased core body temperature, a result that is in accordance with the significant differences in cycle 4 of SWAmean and findings of Badia et al. (15). This prominent effect on NREMS-SWA30 min (p < 0.05; paired t test). An anal- temperature was accompanied by only minor changes ysis of consecutive 5-minute intervals revealed that of sleep and the EEG. In contrast to the increase in the significant change in cycle 4 occurred in the last sleep latency after BL, the REMS latency was not aftwo 5-minute intervals of the first 30 minutes. Aver- fected. Although the REMS latencies in DL were rather aged over the entire sleep episode, SWAin NREMS short, they are within the range of normal healthy young did not differ significantly between conditions (DL = subjects when they are well adapted to. the laboratory 100%; BL = 103.4%; Table O. (27). There were no significant differences in the sleep The rise rate of SWAin the first 30 minutes in each stages, and the typical decline of SWA over successive of the four NREMS episodes (NREMS-SWArise) was cycles was similar under both experimental conditions estimated by calculating for each individual the me- (Fig. 1). For the entire sleep episode, SW A as well as dian of the differences in SWA over consecutive power density in the other frequency bands showed no 5-minute intervals (24). A repeated measure ANOVA significant differences between the conditions. Nev(two factors: condition, cycle) revealed a significant ertheless, small but significant differences in the time effect of cycle (F3•18 = 21.17; P < 0.001), no effect of course of SWA were present. In the first NREMS.,.. Sleep. Vol. 15. No.4. 1992
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.~.
TABLE 3. Slow-wave activity (SWA) and rectal temperature parameters/or the NREMS-REMS cycles Cycle Parameter SWAme"o (%)
NREMS-SWA30minb (%) NREMS-SWAri~e
(%)
Tempmean d ("C)
Condition
I
2
DL BL
189.0 (8.5) 165.1 (16.5) 147.8 (10.7) 153.8 (17.2) 34.1(1.7) 36.5 (5.7)
122.1 (12.6) 129.6 (14.9)
DL BL DL BL DL BL DL BL
35.8 (0.1)** 36.1 (0.1 )** -10.5 (7.2) -15.4 (3.1)
3
4
70.3 (9.1) 85.2 (5.0) 52.8 (7.1) 64.2 (9.4)
44.7 (4.1)* 64.6 (9.2)*
10.9 (3.0) 11.6(1.7)
6.0 (0.9) 10.9 (2.4)
35.7 (0.1)** 36.0 (0.1)**
35.8 (0.1)** 36.1 (0.1 )**
36.0 (0.1) 36.0 (0.1)
0.5 (1.9) 0.0 (2.4)
6.7 (2.7) 2.4 (2.9)
1.6 (3.4) 1.5 (2.4)
81.4 (11.5) 94.8 (12.9) 20.8 (4.6) 19.9 (5.1)
39.0 (3.1)* 51.7 (6.0)*
° Mean SWAin NREMS. b Mean SWAin the first 30 minutes of the NREMS episode. e The interindividual mean of the intraindividual median valUl! of the differences in SWA over consecutive 5-minute intervals in the first 30 minutes of a NREMS episode. d Mean rectal temperature ("C) per cycle. 20 e Change in rectal temperature over the first 30 minutes of the NREMS episode (1O- C); difference between the mean 5-minute value preceding the episode and the mean value of the 25-30-minute interval. All SWA parameters are expressed as a percentage of the mean SWA in NREMS (100%). Significant differences between BL and DL are indicated by *p < 0.05 and **p < 0.01 (paired t test).
REMS cycle, power density in a frequency bin within the delta range was lower in BL than in DL. Conversely, an increase in delta activity was present in the fourth cycle. This shift in the distribution ofSWA could have been caused by a slight suppression in the first cycle as a consequence of BL and a rebound during later parts of sleep. A similar intra sleep rebound has been induced after the selective suppression of SWAby acoustic stimuli in the first 3 hours of sleep (28). The higher rise rate of SWA in the fourth NREMS episode is an indication that "sleep pressure" in the later part of sleep was higher in BL than in DL (24). On the other hand, it is more difficult to specify the factor that led to the slight initial suppression of SWAin BL. Although the longer sleep latency is consistent with a sleep-disturbing aftereffect of BL, the rise rate in the first NREMS episode was not altered (Table 3). It may be the somewhat earlier initiation ofREMS in BL (Fig. 2) that gave rise to a curtailment of SWAin the first cycle and a compensatory increase in cycle 4. The present study provided the opportunity of comparing the dynamics of SWA and rectal temperature. It had been reported that the elevation of body temperature during waking to values that are at the limit or above values that occur under physiological conditions enhance SWS (17-19). Other authors proposed that a regulated rapid decline in core body temperature after sleep onset is a necessary prerequisite for sustained SWS (29). The present data do not support the assumption of a close relationship between body temperature on the one hand and either SWS or SWA on the other hand. The higher body temperature in BL during the hours preceding sleep (16) did not affect Sleep, Vol. 15, No.4, 1992
SWS, and, if anything, reduced SWA in the first NREMS-REMS cycle. As has been mentioned, the slight increase of SWAin cycle 4 constituted probably a compensatory response. However, the possibility that it may have been due to a delayed effect of the heat load cannot be excluded. There was no indication that the rate of initial temperature decline was related to SWS or SWA. If anything, the slight reduction ofSW A in the first cycle of BL was associated with a steeper decline of rectal temperature (Table 3). This weak relationship between SWS/SWA and body temperature is in accordance with Dijk et al. (30) who found a dissociation between the time course ofSW A and body temperature. In conclusion, exposure to BL prior to sleep constitutes a subtle method for elevating body temperature at sleep onset and during the first part of sleep. This effect is mediated via the eyes rather than by the radiant heat of light (16) and must be due to an action on mechanisms subserving thermoregulation and/or circadian rhythmicity. Processes underlying sleep homeostasis are apparently little affected when body temperature is manipulated within a physiological range. Acknowledgements: We thank Dr. I. Tobler and Dr. P. Achermann for their comments and Dr. M. MUnch for her assistance in data acquisition. The study was supported by the Swiss National Science Foundation, grant no. 3125634.88.
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