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. 2008 Aug;23(4):353-61.
doi: 10.1177/0748730408318081.

An endogenous circadian rhythm in sleep inertia results in greatest cognitive impairment upon awakening during the biological night

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An endogenous circadian rhythm in sleep inertia results in greatest cognitive impairment upon awakening during the biological night

Frank A J L Scheer et al. J Biol Rhythms. 2008 Aug.

Abstract

Sleep inertia is the impaired cognitive performance immediately upon awakening, which decays over tens of minutes. This phenomenon has relevance to people who need to make important decisions soon after awakening, such as on-call emergency workers. Such awakenings can occur at varied times of day or night, so the objective of the study was to determine whether or not the magnitude of sleep inertia varies according to the phase of the endogenous circadian cycle. Twelve adults (mean, 24 years; 7 men) with no medical disorders other than mild asthma were studied. Following 2 baseline days and nights, subjects underwent a forced desynchrony protocol composed of seven 28-h sleep/wake cycles, while maintaining a sleep/wakefulness ratio of 1:2 throughout. Subjects were awakened by a standardized auditory stimulus 3 times each sleep period for sleep inertia assessments. The magnitude of sleep inertia was quantified as the change in cognitive performance (number of correct additions in a 2-min serial addition test) across the first 20 min of wakefulness. Circadian phase was estimated from core body temperature (fitted temperature minimum assigned 0 degrees ). Data were segregated according to: (1) circadian phase (60 degrees bins); (2) sleep stage; and (3) 3rd of the night after which awakenings occurred (i.e., tertiary 1, 2, or 3). To control for any effect of sleep stage, the circadian rhythm of sleep inertia was initially assessed following awakenings from Stage 2 (62% of awakening occurred from this stage; n = 110). This revealed a significant circadian rhythm in the sleep inertia of cognitive performance (p = 0.007), which was 3.6 times larger during the biological night (circadian bin 300 degrees , approximately 2300-0300 h in these subjects) than during the biological day (bin 180 degrees , approximately 1500-1900 h). The circadian rhythm in sleep inertia was still present when awakenings from all sleep stages were included (p = 0.004), and this rhythm could not be explained by changes in underlying sleep drive prior to awakening (changes in sleep efficiency across circadian phase or across the tertiaries), or by the proportion of the varied sleep stages prior to awakenings. This robust endogenous circadian rhythm in sleep inertia may have important implications for people who need to be alert soon after awakening.

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Figures

Figure 1
Figure 1
Study protocol. (Top) Schematic example of the forced desynchrony (FD) protocol for a subject with a habitual wake time at 0800 h. Thick horizontal black bars depict scheduled sleep opportunities; vertical gray bars indicate times of sleep inertia testing. Days 1 and 2 are the baseline days, after which seven 28-h “days” occur. The scheduled sleep periods are evenly distributed across all circadian phases. (Bottom) Sequence of tests immediately following awakenings from sleep. Subjects were awakened by a standardized auditory stimulus and performed a serial addition test 1 to 2 min following awakening and again 20 min following awakening, while remaining awake in a semirecumbent posture. The impairment during the test immediately upon awakening relative to 20 min following awakening was quantified as the measure of the severity of sleep inertia.
Figure 2
Figure 2
Circadian rhythm in sleep inertia of cognitive performance. Cognitive performance immediately upon awakening from stage 2 non-REM sleep exhibited a large amplitude circadian variation (solid black circles). Furthermore, the vertical difference between solid black circles (immediately upon awakening) and open black circles (20 min after awakening)—representing the magnitude of sleep inertia and exemplified by the height of the vertical dashed arrow for 1 circadian phase—also exhibited a significant circadian variation. Measurements taken during the scheduled prolonged wake episodes are shown as open gray squares. On the abscissa, data are aligned according to circadian phase from 0° to 359° (6 “bins,” with 0° = core body temperature minimum). Performance is expressed in absolute units based on the group average (left ordinate) and as a percentage of each individual’s average performance 20 min following awakening (right ordinate). The data represent mean data that are double plotted to aid visualization of rhythmicity. Gray shaded areas indicate the group average time of habitual sleep episodes. Error bars indicate SEM.
Figure 3
Figure 3
Circadian rhythm in sleep inertia and sleep efficiency according to time into sleep episode. Sleep inertia after awakening from combined sleep stages exhibits a similar circadian rhythm amplitude and phase for each of the 3 tertiaries, with a peak at 300°. In contrast, sleep efficiency shows no circadian rhythm during the first tertiary and a very large rhythm during the last tertiary. Filled symbols indicate the increase in number of correct additions across the first 20 min following awakening as a measure of dissipation of sleep inertia. Open symbols indicate sleep efficiency (total sleep time as a percentage of scheduled sleep episode). Error bars indicate SEM; n = 9 subjects (3 subjects were excluded due to incomplete data, e.g., due to inhaler use).

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