Differential effects of split and continuous sleep on neurobehavioral function and glucose tolerance in sleep-restricted adolescents

Abstract

Study objectives: Many adolescents are exposed to sleep restriction on school nights. We assessed how different apportionment of restricted sleep (continuous vs. split sleep) influences neurobehavioral function and glucose levels.

Methods: Adolescents, aged 15-19 years, were evaluated in a dormitory setting using a parallel-group design. Following two baseline nights of 9-hour time-in-bed (TIB), participants underwent either 5 nights of continuous 6.5-h TIB (n = 29) or 5-hour nocturnal TIB with a 1.5-hour afternoon nap (n = 29). After two recovery nights of 9-hour TIB, participants were sleep restricted for another three nights. Sleep was assessed using polysomnography (PSG). Cognitive performance and mood were evaluated three times per day. Oral glucose tolerance tests (OGTT) were conducted on mornings after baseline sleep, recovery sleep, and the third day of each sleep restriction cycle.

Results: The split sleep group had fewer vigilance lapses, better working memory and executive function, faster processing speed, lower level of subjective sleepiness, and more positive mood, even though PSG-verified total sleep time was less than the continuous sleep group. However, vigilance in both sleep-restricted groups was inferior to adolescents in a prior sample given 9-hour nocturnal TIB. During both cycles of sleep restriction, blood glucose during the OGTT increased by a greater amount in the split sleep schedule compared with persons receiving 6.5-hour continuous sleep.

Conclusions: In adolescents, modest multinight sleep restriction had divergent negative effects on cognitive performance and glucose levels depending on how the restricted sleep was apportioned. They are best advised to obtain the recommended amount of nocturnal sleep.

Trial registration: https://clinicaltrials.gov/ct2/show/NCT03333512.

Keywords: adolescents; cognition; continuous sleep; glucose tolerance; partial sleep deprivation; sleep restriction; split sleep; vigilance.

Figure 1.

Protocol. In this 15-day protocol, both (A) the continuous sleep group and (B) the split sleep group had two adaptation and baseline nights (B₁ and B₂; TIB indicated by black bars = 9 hours from 23:00 to 08:00). The first cycle of sleep restriction lasted five nights (SR1₁ to SR1₅) followed by two nights of recovery sleep (R1₁ and R1₂; TIB = 9 hours). The second cycle consisted of three nights of sleep restriction (SR2₁ to SR2₃) and two nights of recovery sleep (R2₁ and R2₂). During the two SR periods, the continuous sleep group had a nocturnal TIB of 6.5 hours (00:15–06:45), whereas the split sleep group had a nocturnal TIB of 5 hours (01:00–06:00) and a 1.5-hour nap opportunity between 14:00 and 15:30. Asterisks mark nocturnal sleep and daytime nap episodes that were monitored with PSG. A cognitive test battery (purple “T”) was administered at 10:00, 16:15, and 20:00, except during the first and last days of the protocol. An OGTT (gray bars) was performed between 08:30 and 11:00 after the last baseline night (B₂), on the third day of the SR periods (SR1₃ and SR2₃), and after the first two nights of recovery (R1₂).

Figure 2.

Sleep duration and macrostructure per 24-hour period. The least square means and standard errors estimated with general linear mixed models are plotted for polysomnographically assessed (A) TST and duration of (B) N1, (C) N2, (D), N3, and (E) REM sleep across each 24-hour period separately for the split sleep group (blue) and the continuous sleep group (red). Gray shaded areas mark the SR periods. *** p < 0.001, ** p < 0.01, and * p < 0.05 for significant group contrasts.

Figure 3.

Markers of homeostatic sleep pressure. The least square means and standard errors of (A) N2 sleep latency and (B) SWA in the first hour of nocturnal sleep from N2 sleep onset are plotted for the split sleep group (blue) and the continuous sleep group (red) from the second baseline night (B₂) to the first and second cycles of SR (gray shaded areas) and recovery (R). *** p < 0.001, ** p < 0.01, and * p < 0.05 for significant group contrasts.

Figure 4.

Vigilance performance during repeated sleep restriction with a split or continuous sleep schedule. The numbers of lapses in the PVT are shown (A) averaged across the three tests each day, and separately for tests taken in the (B) morning, (C) afternoon, and (D) evening. PVT results are plotted after the last baseline night (day B₂), during the first cycle of sleep restriction (days SR1₁ to SR1₅; gray shading) and after recovery nights (R1₁ and R1₂), to the second cycle of sleep restriction (days SR2₁ to SR2₃ in gray shading) and recovery sleep (R2₁). Observations for the split sleep group are shown in blue and those for the continuous sleep group in red. For comparison, performance in a control group with 9 hours of TIB for sleep is shown in gray for data collected in a previous study [19]. The least square means and standard errors estimated with general linear mixed models are plotted. *** p < 0.001, ** p < 0.01, and * p < 0.05 for significant contrasts between the split and the continuous sleep groups.

Figure 5.

Blood glucose response in sleep-restricted adolescents. An OGTT was performed on mornings following baseline sleep (B₂), sleep restriction (SR1₃), recovery sleep (R1₂), and re-exposure to sleep restriction (SR2₃). The glucose excursion, defined as the change in blood glucose from the fasting state to 2 hours after the 75-g oral glucose load, is shown for the split sleep group (n = 25; blue bars) and the continuous sleep group (n = 26; red bars). The mean ± standard error is shown. Asterisks (*) indicate significant between-group differences in the glucose response, and hash marks (#) indicate significant within-subject differences between OGTTs.