EEG sleep spectra in older adults across all circadian phases during NREM sleep

Abstract

Study objectives: Healthy aging is associated with changes in sleep-wake regulation, and those changes often lead to problems sleeping, both during the night and during daytime. We aimed to examine the electroencephalographic (EEG) sleep spectra during non-rapid eye movement (NREM) sleep when sleep was scheduled at all times of day.

Design/interventions: After three 24-h baseline (BL) days, participants were scheduled to live on 20-hour "days" consisting of 6.7 hours of bed rest and 13.3 hours of wakefulness for 12 consecutive days (forced desynchrony, FD). The EEG was recorded from a central derivation during all scheduled sleep episodes, with subsequent visual scoring and spectral analysis.

Setting: Intensive Physiological Monitoring Unit of the Brigham & Women's Hospital General Clinical Research Center.

Participants: Twenty-four healthy older subjects (64.2 +/- 6.3 yr; 13 women, 11 men)

Measurements and results: Compared with BL nights, EEG activity in the slow wave (0.5 to 5.25 Hz), theta (6 to 6.25 and 7 Hz), alpha (10 to 11.25 Hz), and high spindle range (14.5 to 15.5 Hz) was significantly greater during FD, when subjects slept across many times of day and night. During FD, there was a significant interaction between homeostatic and circadian factors, such that EEG delta activity (0.5 to 1.5 Hz) was higher in the biological morning/early afternoon than at other times. EEG activity was significantly increased in almost all frequency ranges (0.5 to 21 Hz) during the biological day, as compared with the biological night, except for the lower EEG spindle range (12.25 to 14 Hz). Overall, EEG beta activity was positively correlated with wakefulness and negatively correlated with total sleep time.

Conclusion: Our findings provide some new evidence for the underlying mechanisms that contribute to age-related difficulties in sleep consolidation, especially when sleep occurs during the daytime.

Figure 1

Double-raster plot of the 32-day study design. The x-axis represents relative clock time, the y-axis indicates days in the protocol. Black bars indicate scheduled sleep episodes. The first 3 days were 24-hour baseline (BL) days (16 hours wake and 8 hours bedrest), and this was followed by 30 cycles of forced desynchrony (FD) with 13.3 hours wake and 6.7 hours of scheduled bedrest per cycle. Grey boxes represent the 2 conditions of the FD in which the placebo occurred (first 12 FD nights or final 12 FD nights). Three 24-hour recovery days (not included in present analysis) were scheduled at the end of the protocol.

Figure 2

Method used for biological day vs. night assessment. Double-plotted plasma melatonin levels during a 24-hour baseline day, averaged per 15° (∼1 hour). Dashed lines indicate the 25% dim light melatonin on- and offset (DLMOn and DLMOff). Dotted lines delineate segments where endogenous melatonin is higher or lower than 2 SD of daytime levels (N = 23; ± SEM). 0° = CBT minimum.

Figure 3

Circadian and homeostatic polysomnography data from 24 subjects: Upper panel—wakefulness during scheduled sleep; lower panel—total sleep time (TST) (sleep stages 1-4 and rapid eye movement ([REM] sleep) (both graphs are double-plotted). 0° refers to core body temperature minimum. ± SEM (upper panel) and − SEM (lower panel).

Figure 4

Averaged electroencephalographic (EEG) spectra across forced-desynchrony (FD) sleep episodes relative to baseline (BL) (100% = first 6.7 hours of BL) in the frequency range between 0.5 and 25 Hz (black circles, ± SEM). Black triangles indicate frequency bins in which FD is significantly different from BL (main effect of condition), white triangles indicate frequency bins in which there are significant main effects of sex, with women having higher EEG power density values than men. N = 24.

Figure 5

Circadian-dependent (left side; double-plotted) and homeostatic-dependent (right side) electroencephalographic (EEG) activity during forced desynchrony (FD). EEG spectra were averaged across multiple frequency ranges as indicated in the right label: slow-wave activity (SWA): 0.75-4.5 Hz; theta activity: 4.75-7.5 Hz; alpha activity: 8-12 Hz; low spindle frequency activity (LSFA): 12.25-13.75 Hz; high spindle frequency activity (HSFA): 14-15.5 Hz; beta activity: 15.75-24.75 Hz (N = 24; ± SEM). Dotted line at 0° in the left panel indicates the time of the core body temperature minimum.

Figure 6

Interaction of circadian and homeostatic effects in the electroencephalographic (EEG) delta range. EEG delta power (0.5-1.5 Hz) was averaged with respect to circadian phase for each quarter of the scheduled sleep episode and is shown double-plotted. N = 24; ± SEM.

Figure 7

Averaged electroencephalographic (EEG) spectra relative to baseline (100% = first 6.7 hours of baseline) during sleep episodes scheduled in the biological night (upper panel) and biological day (lower panel) for women (filled circles) and men (open circles). Black upward triangles indicate frequency bins in which there are significant sex differences, white triangles indicate frequency bins in which there are significant differences between biological day and night, and black downward triangles indicate frequency bins in which there are significant interactions between sex and day/night condition. N = 23 (13 F, 10 M); ± SEM.

Figure 8

Relationship between electroencephalographic (EEG) beta activity (15.75-20.5 Hz) and total sleep time (TST; upper panel) and wakefulness during scheduled sleep (lower panel) across circadian phases. Filled symbols: EEG beta activity; open symbols: TST or wakefulness during scheduled sleep. Data are expressed as deviation from the mean and are shown averaged with respect to circadian phase and double plotted. N = 24; ± SEM.