Memory performance following napping in habitual and non-habitual nappers

Ruth L F Leong, Nicole Yu, Ju Lynn Ong, Alyssa S C Ng, S Azrin Jamaluddin, James N Cousins, Nicholas I Y N Chee, Michael W L Chee, Ruth L F Leong, Nicole Yu, Ju Lynn Ong, Alyssa S C Ng, S Azrin Jamaluddin, James N Cousins, Nicholas I Y N Chee, Michael W L Chee

Abstract

Study objectives: Afternoon naps benefit memory but this may depend on whether one is a habitual napper (HN; ≥1 nap/week) or non-habitual napper (NN). Here, we investigated whether a nap would benefit HN and NN differently, as well as whether HN would be more adversely affected by nap restriction compared to NN.

Methods: Forty-six participants in the nap condition (HN-nap: n = 25, NN-nap: n = 21) took a 90-min nap (14:00-15:30 pm) on experimental days while 46 participants in the Wake condition (HN-wake: n = 24, NN-wake: n = 22) remained awake in the afternoon. Memory tasks were administered after the nap to assess short-term topographical memory and long-term memory in the form of picture encoding and factual knowledge learning respectively.

Results: An afternoon nap boosted picture encoding and factual knowledge learning irrespective of whether one habitually napped (main effects of condition (nap/wake): ps < 0.037). However, we found a significant interaction for the hippocampal-dependent topographical memory task (p = 0.039) wherein a nap, relative to wake, benefitted habitual nappers (HN-nap vs HN-wake: p = 0.003) compared to non-habitual nappers (NN-nap vs. NN-wake: p = 0.918). Notably for this task, habitual nappers' performance significantly declined if they were not allowed to nap (HN-wake vs NN-wake: p = 0.037).

Conclusions: Contrary to concerns that napping may be disadvantageous for non-habitual nappers, we found that an afternoon nap was beneficial for long-term memory tasks even if one did not habitually nap. Naps were especially beneficial for habitual nappers performing a short-term topographical memory task, as it restored the decline that would otherwise have been incurred without a nap.

Clinical trial information: NCT04044885.

Keywords: adolescents; habitual; learning; memory; naps.

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

Figures

Figure 1.
Figure 1.
Memory task protocols. All encoding sessions were performed at 16:45 pm, approximately 75 min after the nap period (14:00–15:30 pm). In the Four Mountains Task (4MT), encoding was immediately followed by retrieval. For the picture encoding task, the retrieval session was performed after two nights of 9 h nocturnal time in bed (TIB). Encoding sessions for the factual knowledge task took place across 3 days, with encoding of material occurring after the nap period. The retrieval session took place in the evening (20:30 pm) of the next rest day. Asterisks indicate the naps in which sleep was assessed with polysomnography.
Figure 2.
Figure 2.
Nap sleep parameters assessed across polysomnography-monitored experimental naps: M13 (third day of the first manipulation cycle, Four Mountains Task), M15 (fifth day of the first manipulation cycle, picture encoding task), M21 and M23 (first and third days of the second manipulation cycle [no PSG performed on M22], factual knowledge task). Means and standard errors are plotted separately for habitual nappers (solid line) and non-habitual nappers (dashed line) for total sleep time (TST) and duration of N1, N2, N3, and rapid-eye-movement (REM) sleep across each experimental nap period. *p < 0.05.
Figure 3.
Figure 3.
Four Mountains Task (4MT) performance for habitual (gray bars) and non-habitual nappers (white bars) in the experimental nap and wake conditions. Means and standard errors of the mean for the percentage of correct trials are plotted. *p < 0.05.

References

    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. Mednick S, et al. . Sleep-dependent learning: a nap is as good as a night. Nat Neurosci. 2003;6(7):697–698.
    1. Ficca G, et al. . Naps, cognition and performance. Sleep Med Rev. 2010;14(4):249–258.
    1. Lovato N, et al. . The effects of napping on cognitive functioning. Prog Brain Res. 2010;185:155–166.
    1. Mantua J, et al. . Exploring the nap paradox: are mid-day sleep bouts a friend or foe? Sleep Med. 2017;37:88–97.
    1. Cousins JN, et al. . A split sleep schedule rescues short-term topographical memory after multiple nights of sleep restriction. Sleep. 2019;42(4). doi: 10.1093/sleep/zsz018
    1. Lemos N, et al. . Naps in school can enhance the duration of declarative memories learned by adolescents. Front Syst Neurosci. 2014;8:103.
    1. Cellini N, et al. . Sleep before and after learning promotes the consolidation of both neutral and emotional information regardless of REM presence. Neurobiol Learn Mem. 2016;133:136–144.
    1. Nishida M, et al. . Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS One. 2007;2(4):e341.
    1. van der Helm E, et al. . REM sleep depotentiates amygdala activity to previous emotional experiences. Curr Biol. 2011;21(23):2029–2032.
    1. Ong JL, et al. . A daytime nap restores hippocampal function and improves declarative learning. Sleep. 2020;43(9). doi: 10.1093/sleep/zsaa058.
    1. Mander BA, et al. . Wake deterioration and sleep restoration of human learning. Curr Biol. 2011;21(5):R183–R184.
    1. Alger SE, et al. . Challenging the stigma of workplace napping. Sleep. 2019;42(8). doi: 10.1093/sleep/zsz097.
    1. Foundation NS.Sleep in America Poll: Communications Technology and Sleep. Washington (DC): National Sleep Foundation; 2011.
    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. Thorleifsdottir B, et al. . Sleep and sleep habits from childhood to young adulthood over a 10-year period. J Psychosom Res. 2002;53(1):529–537.
    1. Fischer FM, et al. . Explaining sleep duration in adolescents: the impact of socio-demographic and lifestyle factors and working status. Chronobiol Int. 2008;25(2):359–372.
    1. Jakubowski KP, et al. . Temporal relationships between napping and nocturnal sleep in healthy adolescents. Behav Sleep Med. 2017;15(4):257–269.
    1. Duggan KA, et al. . To nap, perchance to DREAM: a factor analysis of college students’ self-reported reasons for napping. Behav Sleep Med. 2018;16(2):135–153.
    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. Vela-Bueno A, et al. . Sleep and behavioral correlates of napping among young adults: a survey of first-year university students in Madrid, Spain. J Am Coll Health. 2008;57(2):150–158.
    1. Schoen LS, et al. . Facilitated recall following REM and NREM naps. Psychophysiology. 1984;21(3):299–306.
    1. Wilhelm I, et al. . Opposite effects of cortisol on consolidation of temporal sequence memory during waking and sleep. J Cogn Neurosci. 2011;23(12):3703–3712.
    1. Doyon J, et al. . Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning. Exp Brain Res. 2009;195(1):15–26.
    1. Hoedlmoser K, et al. . The impact of diurnal sleep on the consolidation of a complex gross motor adaptation task. J Sleep Res. 2015;24(1):100–109.
    1. Ruch S, et al. . Sleep stage II contributes to the consolidation of declarative memories. Neuropsychologia. 2012;50(10):2389–2396.
    1. Tietzel AJ, et al. . The short-term benefits of brief and long naps following nocturnal sleep restriction. Sleep. 2001;24(3):293–300.
    1. Dinges DF. Adult napping and its effects on ability to function. In: Stampi C., ed. Why We Nap: Evolution, Chronobiology, and Functions of Polyphasic and Ultrashort Sleep. Boston, MA: Birkhäuser; 1992.
    1. McDevitt EA, et al. . The effect of nap frequency on daytime sleep architecture. Physiol Behav. 2012;107(1):40–44.
    1. Spiegel R. Sleep and sleeplessness in advanced age. Adv Sleep Res. 1981;5:1–272.
    1. Evans FJ, et al. . Appetitive and replacement naps: EEG and behavior. Science. 1977;197(4304):687–689.
    1. Milner CE, et al. . Habitual napping moderates motor performance improvements following a short daytime nap. Biol Psychol. 2006;73(2):141–156.
    1. McDevitt EA, et al. . The impact of frequent napping and nap practice on sleep-dependent memory in humans. Sci Rep. 2018;8(1):15053.
    1. Kurdziel L, et al. . Sleep spindles in midday naps enhance learning in preschool children. Proc Natl Acad Sci USA. 2013;110(43):17267–17272.
    1. Hagenauer MH, et al. . Adolescent changes in the homeostatic and circadian regulation of sleep. Dev Neurosci. 2009;31(4):276–284.
    1. Taylor DJ, et al. . Sleep tendency during extended wakefulness: insights into adolescent sleep regulation and behavior. J Sleep Res. 2005;14(3):239–244.
    1. Cousins JN, et al. . The long-term memory benefits of a daytime nap compared with cramming. Sleep. 2019;42(1). doi: 10.1093/sleep/zsy207
    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. Lo JC, et al. . Cognitive effects of split and continuous sleep schedules in adolescents differ according to total sleep opportunity. Sleep. 2020;43(12). doi: 10.1093/sleep/zsaa129
    1. Raven J.Advanced Progressive Matrices: Set II (1962 Revision). London: H. K. Lewis; 1978.
    1. Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991;14(6):540–545.
    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. 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. Beck AT, et al. . Manual for the Beck Depression Inventory-II. San Antonio. TX: Psychological Corporation; 1996.
    1. Beck AT, et al. . Beck Anxiety Inventory Manual. San Antonio, TX: Harcourt Brace and Company; 1993.
    1. Iber C, et al. . The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology, and Technical Specifications. 1st ed.Westchester, IL: American Academy of Sleep Medicine; 2007.
    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. Ong JL, et al. . EEG changes across multiple nights of sleep restriction and recovery in adolescents: the need for sleep study. Sleep. 2016;39(6):1233–1240.
    1. Welch P. The use of the fast Fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms. IEEE T Acoust Speech 1967;15:70–73.
    1. Mölle M, et al. . Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing. Sleep. 2011;34(10):1411–1421.
    1. Hartley T, et al. . The hippocampus is required for short-term topographical memory in humans. Hippocampus. 2007;17(1):34–48.
    1. Hartley T, et al. . An association between human hippocampal volume and topographical memory in healthy young adults. Front Hum Neurosci. 2012;6:338.
    1. Takashima A, et al. . Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. Proc Natl Acad Sci USA. 2006;103(3):756–761.
    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. Cousins JN, et al. . Does splitting sleep improve long-term memory in chronically sleep deprived adolescents? NPJ Sci Learn. 2019;4:8.
    1. Rasch B, et al. . About sleep’s role in memory. Physiol Rev. 2013;93(2):681–766.
    1. Piosczyk H, et al. . The effect of sleep-specific brain activity versus reduced stimulus interference on declarative memory consolidation. J Sleep Res. 2013;22(4):406–413.
    1. Alger SE, et al. . Delayed onset of a daytime nap facilitates retention of declarative memory. PLoS One. 2010;5(8):e12131.
    1. O’Keefe J. Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus. 1999;9(4):352–364.
    1. Bird CM, et al. . Topographical short-term memory differentiates Alzheimer’s disease from frontotemporal lobar degeneration. Hippocampus. 2010;20(10):1154–1169.
    1. Chan D, et al. . The 4 mountains test: a short test of spatial memory with high sensitivity for the diagnosis of pre-dementia Alzheimer’s disease. J Vis Exp. 2016;( 116):54454.
    1. Moodley K, et al. . Diagnostic differentiation of mild cognitive impairment due to Alzheimer’s disease using a hippocampus-dependent test of spatial memory. Hippocampus. 2015;25(8):939–951.
    1. Pengas G, et al. . Lost and found: bespoke memory testing for Alzheimer’s disease and semantic dementia. J Alzheimer’s Dis. 2010;21(4):1347–1365.
    1. Tononi G, et al. . Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull. 2003;62(2):143–150.
    1. Vyazovskiy VV, et al. . Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat Neurosci. 2008;11(2):200–208.
    1. Cousins JN, et al. . The impact of sleep deprivation on declarative memory. Prog Brain Res. 2019;246:27–53.
    1. Carskadon MA, et al. . Multiple sleep latency tests during the constant routine. Sleep. 1992;15(5):396–399.
    1. Broughton RJ, et al. . Napping: a ubiquitous enigma. In: Dinges DF, Broughton RJ, eds. Sleep and Alertness: Chronobiological, Behavioural, and Medical Aspects of Napping. New York, NY: Raven Press; 1989:1–7.
    1. Yeo SC, et al. . Associations of time spent on homework or studying with nocturnal sleep behavior and depression symptoms in adolescents from Singapore. Sleep Health. 2020;6(6):758–766.
    1. Lo JC, et al. . Sustained benefits of delaying school start time on adolescent sleep and well-being. Sleep. 2018;41(6). doi: 10.1093/sleep/zsy052
    1. Minges KE, et al. . Delayed school start times and adolescent sleep: a systematic review of the experimental evidence. Sleep Med Rev. 2016;28:86–95.

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