Cognitive effects of split and continuous sleep schedules in adolescents differ according to total sleep opportunity

June C Lo, Ruth L F Leong, Alyssa S C Ng, S Azrin Jamaluddin, Ju Lynn Ong, Shohreh Ghorbani, TeYang Lau, Nicholas I Y N Chee, Joshua J Gooley, Michael W L Chee, June C Lo, Ruth L F Leong, Alyssa S C Ng, S Azrin Jamaluddin, Ju Lynn Ong, Shohreh Ghorbani, TeYang Lau, Nicholas I Y N Chee, Joshua J Gooley, Michael W L Chee

Abstract

Study objectives: We compared the basic cognitive functions of adolescents undergoing split (nocturnal sleep + daytime nap) and continuous nocturnal sleep schedules when total sleep opportunity was either below or within the recommended range (i.e. 6.5 or 8 h).

Methods: Adolescent participants (age: 15-19 year) in the 8-h split (n = 24) and continuous (n = 29) sleep groups were compared with 6.5-h split and continuous sleep groups from a previous study (n = 58). These protocols involved two baseline nights (9-h time-in-bed [TIB]), 5 nights of sleep manipulation, 2 recovery nights (9-h TIB), followed by a second cycle of sleep manipulation (3 nights) and recovery (2 nights). Cognitive performance, subjective sleepiness, and mood were evaluated daily; sleep was assessed using polysomnography.

Results: Splitting 6.5 h of sleep with a mid-afternoon nap offered a boost to cognitive function compared to continuous nocturnal sleep. However, when total TIB across 24 h increased to 8 h, the split and continuous sleep groups performed comparably in tests evaluating vigilance, working memory, executive function, processing speed, subjective sleepiness, and mood.

Conclusions: In adolescents, the effects of split sleep on basic cognitive functions vary by the amount of total sleep obtained. As long as the total sleep opportunity across 24 h is within the recommended range, students may fulfill sleep requirements by adopting a split sleep schedule consisting of a shorter period of nocturnal sleep combined with a mid-afternoon nap, without significant impact on basic cognitive functions.

Clinical trial registration: NCT04044885.

Keywords: adolescents; cognition; continuous sleep; naps; split sleep; vigilance.

© Sleep Research Society 2020. Published by Oxford University Press on behalf of the Sleep Research Society.

Figures

Figure 1.
Figure 1.
Protocol. In this 15-day protocol, both the 8-h split sleep group and the 8-h split continuous group had two adaptation and baseline nights (B1 and B2; TIB indicated by black bars = 9 h from 11:00 pm to 08:00 am). The first cycle of sleep opportunity manipulation lasted 5 nights (M11–M15) followed by two nights of recovery sleep (R11 and R12; TIB = 9 h). The second cycle consisted of three manipulation nights (M21–M23) and two recovery nights (R21 and R22). During the two sleep opportunity manipulation periods, the split sleep group had a nocturnal TIB of 6.5 h (00:15 am–06:45 am) and a 1.5-h nap opportunity between 2:00 pm and 3:30 pm, while the continuous sleep group had a nocturnal TIB of 8 h (11:30 pm–07:30 am). Asterisks indicate nocturnal sleep and daytime nap episodes with polysomnographic recordings. A cognitive test battery (yellow bars) was administered at 10:00 am, 4:15 pm, and 8:00 pm daily, except during the first and last days of the protocol.
Figure 2.
Figure 2.
Sleep duration and macrostructure per 24-h 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) rapid-eye-movement (REM) sleep across each 24-h period separately for the 8-h split sleep group (red open circles and dotted line) and the 8-h continuous sleep group (red filled circles and solid line) during the second baseline night (B2), the sleep opportunity manipulation nights (M; gray shaded areas), and the recovery nights (R). ***p < 0.001, **p < 0.01, and *p < 0.05 for significant group contrasts.
Figure 3.
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 8-h split sleep group (red open circles and dotted line) and the 8-h continuous sleep group (red filled circles and solid line) from the second baseline night (B2) to the first and second cycles of sleep opportunity manipulation (M; gray shaded areas) and recovery (R). ***p < 0.001, **p < 0.01, and *p < 0.05 for significant group contrasts.
Figure 4.
Figure 4.
Vigilance performance during a split or continuous sleep schedule when total TIB was below or within the recommended range. 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 opportunity manipulation (days M11–M15; gray shading) and after recovery nights (R11 and R12), to the second cycle of sleep manipulation (days M21–M23 in gray shading) and recovery sleep (R21). Observations for the 8-h split sleep group are shown in red open circles and dotted lines, while those for the 8-h continuous sleep group are illustrated in red filled circles and solid lines. For comparison, performance in a 6.5-h split sleep group (blue open circles and dotted lines) and a 6.5-h continuous sleep group (blue filled circles and solid lines) from a previous study [13] are also presented. 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 (red for the two 8-h sleep groups and blue for the two 6.5-h sleep groups).
Figure 5.
Figure 5.
Other neurobehavioral functions during a split or continuous sleep schedule when total TIB was below or within the recommended range. The least square means and standard errors estimated with general linear mixed models are plotted for the daily average in (A) the number of correct responses in the MAT and the SDMT as measures of speed of processing, (B) A’ in the 1- and 3-back tasks as measures of working memory/executive function, (C) the score on the KSS as a measure of subjective sleepiness, and (D) the positive and negative affect scores on the PANAS. Data on the last baseline day (B2), as well as during the sleep opportunity manipulation periods (M; gray shading) and the recovery periods (R) are plotted in red open circles and dotted lines for the 8-h split sleep group and red filled circles and solid lines for the 8-h continuous sleep group. For comparison, performance in a 6.5-h split sleep group (blue open circles and dotted lines) and a 6.5-h continuous sleep group (blue filled circles and solid lines) from a previous study [13] also illustrated. ***p < 0.001, **p < 0.01, and *p < 0.05 for significant contrasts between the split and the consolidated sleep groups (red for the two 8-h sleep groups and blue for the two 6.5-h sleep groups).

References

    1. Jiang X, et al. Sleep duration, schedule and quality among urban Chinese children and adolescents: associations with routine after-school activities. PLoS One. 2015;10(1):e0115326.
    1. Patte KA, et al. Modifiable predictors of insufficient sleep durations: a longitudinal analysis of youth in the COMPASS study. Prev Med. 2018;106:164–170.
    1. Twenge JM, et al. Decreases in self-reported sleep duration among U.S. adolescents 2009–2015 and association with new media screen time. Sleep Med 2017;39:47–53.
    1. Yeo SC, et al. Associations of sleep duration on school nights with self-rated health, overweight, and depression symptoms in adolescents: problems and possible solutions. Sleep Med. 2019;60:96–108.
    1. Hirshkowitz M, et al. National Sleep Foundation’s sleep time duration recommendations: methodology and results summary. Sleep Health. 2015;1(1):40–43.
    1. Paruthi S, et al. Recommended amount of sleep for pediatric populations: a consensus statement of the American academy of sleep medicine. J Clin Sleep Med. 2016;12(6):785–786.
    1. Carskadon MA. Sleep in adolescents: the perfect storm. Pediatr Clin North Am. 2011;58(3):637–647.
    1. Crowley SJ, et al. A longitudinal assessment of sleep timing, circadian phase, and phase angle of entrainment across human adolescence. PLoS One. 2014;9(11):e112199.
    1. Jenni OG, et al. Homeostatic sleep regulation in adolescents. Sleep. 2005;28(11):1446–1454.
    1. Yeo SC, et al. Associations of time spent on homework or studying with nocturnal sleep behaviour and depression symptoms in adolescents from Singapore. Sleep Health 2020; (in press). 10.1016/j.sleh.2020.04.011.
    1. Adolescent Sleep Working G, et al.. School start times for adolescents. Pediatrics 2014;134:642–649.
    1. Watson NF, et al. Delaying middle school and high school start times promotes student health and performance: an American academy of sleep medicine position statement. J Clin Sleep Med. 2017;13(4):623–625.
    1. Lo JC, et al. Differential effects of split and continuous sleep on neurobehavioral function and glucose tolerance in sleep-restricted adolescents. Sleep 2019;42(5). doi:10.1093/sleep/zsz037
    1. Ong JL, et al. EEG changes accompanying successive cycles of sleep restriction with and without naps in adolescents. Sleep 2017;40(4). doi:10.1093/sleep/zsx030.
    1. Jackson ML, et al. Investigation of the effectiveness of a split sleep schedule in sustaining sleep and maintaining performance. Chronobiol Int. 2014;31(10):1218–1230.
    1. Kosmadopoulos A, et al. The effects of a split sleep-wake schedule on neurobehavioural performance and predictions of performance under conditions of forced desynchrony. Chronobiol Int. 2014;31(10):1209–1217.
    1. Cousins JN, et al. Memory encoding is impaired after multiple nights of partial sleep restriction. J Sleep Res. 2018;27(1):138–145.
    1. Lo JC, et al. Cognitive performance, sleepiness, and mood in partially sleep deprived adolescents: the need for sleep study. Sleep. 2016;39(3):687–698.
    1. Lo JC, et al. Neurobehavioral impact of successive cycles of sleep restriction with and without naps in adolescents. Sleep 2017;40(2). doi:10.1093/sleep/zsw042.
    1. Horne JA, et al. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol. 1976;4(2):97–110.
    1. Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991;14(6):540–545.
    1. Meijer AM. Chronic sleep reduction, functioning at school and school achievement in preadolescents. J Sleep Res. 2008;17(4):395–405.
    1. Buysse DJ, et al. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193–213.
    1. Patanaik A, et al. An end-to-end framework for real-time automatic sleep stage classification. Sleep 2018;41(5). doi:10.1093/sleep/zsy041.
    1. Iber C, et al. The AASM manual for the scoring of sleep and associated events: rules, terminology, and technical specification. 1st ed. Westchester, IL: American Academy of Sleep Medicine, 2007.
    1. Akerstedt T, et al. Subjective and objective sleepiness in the active individual. Int J Neurosci. 1990;52(1–2):29–37.
    1. Smith A. Symbol Digit Modalities Test. Los Angeles, CA: Western Psychological Services, 1991.
    1. Lo JC, et al. Effects of partial and acute total sleep deprivation on performance across cognitive domains, individuals and circadian phase. PLoS One. 2012;7(9):e45987.
    1. Klein KE, et al. Air operations and circadian performance rhythms. Aviat Space Environ Med. 1976;47(3):221–230.
    1. Watson D, et al. Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol. 1988;54(6):1063–1070.
    1. Dinges DF, Powell JW. Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations. Behav Res Meth Instr Comp. 1985;17:652–655.
    1. Mollicone DJ, et al. Response Surface mapping of neurobehavioral performance: testing the feasibility of split sleep schedules for space operations. Acta Astronaut. 2008;63(7–10):833–840.
    1. Short MA, et al. The effect of split sleep schedules (6h-on/6h-off) on neurobehavioural performance, sleep and sleepiness. Appl Ergon. 2016;54:72–82.
    1. Belenky G, et al. Patterns of performance degradation and restoration during sleep restriction and subsequent recovery: a sleep dose-response study. J Sleep Res. 2003;12(1):1–12.
    1. Belenky G, et al. Split sleeper berth use and driver performance: a review of the literature and application of a mathematical model predicting performance from sleep/wake history and circadian phase. Spokane, WA: Washington State University, 2008.
    1. Campbell IG, et al. Differential and interacting effects of age and sleep restriction on daytime sleepiness and vigilance in adolescence: a longitudinal study. Sleep 2018;41(12). doi:10.1093/sleep/zsy177.
    1. Talbot LS, et al. Sleep deprivation in adolescents and adults: changes in affect. Emotion. 2010;10(6):831–841.
    1. Leong RLF, et al. Multiple nights of partial sleep deprivation do not affect prospective remembering at long delays. Sleep Med. 2018;44:19–23.
    1. Voderholzer U, et al. Sleep restriction over several days does not affect long-term recall of declarative and procedural memories in adolescents. Sleep Med. 2011;12(2):170–178.
    1. Cousins JN, et al. Does splitting sleep improve long-term memory in chronically sleep deprived adolescents? NPJ Sci Learn. 2019;4:8.
    1. Alger SE, et al. Slow wave sleep during a daytime nap is necessary for protection from subsequent interference and long-term retention. Neurobiol Learn Mem. 2012;98(2):188–196.
    1. Mander BA, et al. Wake deterioration and sleep restoration of human learning. Curr Biol. 2011;21(5):R183–R184.
    1. Milner CE, et al. Benefits of napping in healthy adults: impact of nap length, time of day, age, and experience with napping. J Sleep Res. 2009;18(2):272–281.
    1. Werth E, et al. Dynamics of the sleep EEG after an early evening nap: experimental data and simulations. Am J Physiol. 1996;271(3 Pt 2):R501–R510.

Source: PubMed

3
Prenumerera