Napping
Napping
Journal of Adolescence
journal homepage: www.elsevier.com/locate/adolescence
A R T IC LE I N F O ABS TRA CT
Keywords: This study aimed to examine the sleep-dependent memory consolidation of verbal declarative
Sleep memory in Chinese adolescents in a naturalistic experimental setting. Thirty-nine healthy
Memory consolidation boarding school students (ages 15–18, 70% female) were randomized to either a one-hour
Napping afternoon nap or wake group between the baseline and the retest sessions of three verbal de-
Adolescents
clarative memory tasks: a Prose Stories Recall task, a Word Pair Associates task, and Rey Auditory
Verbal memory
Learning
Verbal Learning Test. Results showed that the nap group performed better than the no-nap group
on both the Prose Stories Recall task and the Word Pair Associates task, but not on list learning.
Our findings suggest that napping is beneficial to verbal declarative memory in adolescents,
providing ecologically-valid empirical support for the sleep-dependent memory consolidation
hypothesis using a napping paradigm in participants' naturalistic habitat. Our results demon-
strate the potential importance of napping as a practical mnemonic intervention/compensatory
strategy for student populations.
Previous studies suggest that sleep is important to a multiplicity of cognitive functioning, in particular learning and memory
(Maquet, 2001). The ‘sleep-dependent memory consolidation hypothesis’ suggests that individuals remember more and forget less
when offered a period of sleep over an equivalent period of wake (Stickgold, 2005). Findings supporting this hypothesis have been
established for declarative (Ellenbogen, Hulbert, Stickgold, Dinges, & Thompson-Schill, 2006), procedural (Walker & Stickgold,
2006), and working memory (Lau, Wong, Lau, Hui, & Tseng, 2015; Lo et al., 2012). Whilst it is beyond the scope of this paper to
explore all of the possible mechanisms involved in sleep-dependent memory consolidation, converging evidence from behavioral,
genetic, and neuroimaging studies suggests that offline memory reprocessing during sleep is an important part of how memories are
formed, organized and retrieved (Stickgold, 2005). For example, evidence from fMRI research has shown that a night of sleep
increases activation in brain areas associated with the initial learning of memory tasks, and also shows a positive correlation with
improvement in task performance (Walker, Stickgold, Jolesz, & Yoo, 2005). Studies in rats have also found that several genes believed
to play a role in memory consolidation and brain plasticity are upregulated during sleep (Ribeiro, Goyal, Mello, & Pavlides, 1999).
☆
This article is part of a Special Issue entitled Sleep Issues During Adolescence.
∗
Corresponding author. The Education University of Hong Kong, 10 Lo Ping Road, Tai Po, New Territories, Hong Kong.
E-mail address: [email protected] (E.Y.Y. Lau).
https://doi.org/10.1016/j.adolescence.2018.06.004
Received 16 January 2018; Received in revised form 6 June 2018; Accepted 9 June 2018
Available online 18 June 2018
0140-1971/ © 2018 The Foundation for Professionals in Services for Adolescents. Published by Elsevier Ltd. All rights reserved.
E.Y.Y. Lau et al. Journal of Adolescence 67 (2018) 77–84
For verbal memory, in particular, it has been shown that sleep reduces the negative effect of interfering information on memory
consolidation, which results in greater recall performance after sleep than after an equivalent period of wake (Ellenbogen, Hulbert,
Jiang, & Stickgold, 2009).
Chronic sleep restriction is increasingly common among adolescents worldwide (Gradisar, Gardner, & Dohnt, 2011). The National
Sleep Foundation recommends that teenagers get 8–10 h sleep a night (Hirshkowitz et al., 2015). However, with nightly sleep
averaging 7.5 h in the US (Wolfson & Carskadon, 1998), 7.3 h in Hong Kong (Chung & Cheung, 2008), 6.3 h in Japan (Tagaya et al.,
2004), and 5.4 h in Korea (Yang, Kim, Patel, & Lee, 2005), inadequate sleep seems to be the rule rather than the exception in many
developed countries. Insufficient weekday sleep, coupled with weekend compensatory “sleeping-in”, leads to large weekday-weekend
disparities in sleep duration, which in turn has been reported to predict outcomes such as falling asleep, lower grades and late arrival
to school (Gibson et al., 2006). Late rise times likely result in further delays in sleep phase due to minimized light exposure in the
morning, aggravating nighttime sleep difficulties such as insomnia, and leading to daytime dysfunction such as sleepiness and other
cognitive and affective problems (Fallone, Owens, & Deane, 2002; Gibson et al., 2006). A recent study in a boarding school popu-
lation found that a week of partial sleep deprivation (5 h sleep a night) impaired visual declarative memory in high school adolescents
and that the negative impact continued even after two nights of recovery sleep (Lo, Ong, Leong, Gooley, & Chee, 2016). Not sur-
prisingly, research suggests that sleep disturbance and inadequate sleep are associated with poorer academic results in adolescents
(e.g., Chung & Cheung, 2008; Wong et al., 2013). Unrelenting academic demands, coupled with the ever-increasing use of internet
and online social platforms (Chung & Cheung, 2008; Woods & Scott, 2016), means that students have limited ways and motivation to
improve their nocturnal sleep. Attempts to address this problem (e.g., school-based sleep education) provides immediate short-term
benefits but research suggests improvements in sleep are not sustained (Chung, Chan, Lam, Lai, & Yeung, 2017).
Most studies have established the benefits of sleep on memory by evaluating outcomes following a night of sleep or nighttime
sleep deprivation. However, more recent studies have also investigated the benefits of additional daytime sleep and have found
promising results in declarative (Antonenko, Diekelmann, Olsen, Born, & Mölle, 2013), procedural (Morita, Ogawa, & Uchida, 2012)
and working memory (Lau et al., 2015). Whilst it is difficult to eradicate the negative effects of insufficient sleep by increasing
nighttime sleep, or by delaying school start times, the introduction of daytime naps is a potential way to reduce daytime sleepiness
and maintain learning and academic performance. Indeed, nocturnal sleep and daytime naps were found to have comparable effects
in facilitating memory consolidation (Lo, Dijk, & Groeger, 2014; Tucker & Fishbein, 2009). Whilst daytime napping may not be a
replacement for nocturnal sleep for optimum performance or other psychophysiological functioning, its strategic use in mitigating the
effects of chronic sleep loss, ameliorating the commonly observed circadian rhythm effect of the “post-lunch dip” in alertness
(Broughton, 1989), and improving memory warranted the current investigation.
The aim of the present study was to test the sleep-dependent memory consolidation hypothesis using a napping paradigm in
adolescents, a population prone to chronically-inadequate sleep. Whilst a previous study conducted in a naturalistic setting (boarding
high school) showed that participants who had taken a nap had faster response times and benefitted more from practice than those
who had an equivalent period of wake (Lim, Lo, & Chee, 2017), the current study was the first to investigate the effects of napping in
a similar naturalistic setting on verbal memory consolidation in adolescents. We were interested in verbal declarative memory given
its high relevance to learning. Classroom teaching usually comprises a large amount of information presented verbally. Students'
ability to acquire and retain verbal materials in different formats (e.g., free recall and cued recall) is crucial in the ‘real-life’ learning
of information such as vocabularies and terminologies. We hypothesized that adolescents given a nap opportunity would have
reduced sleepiness and better memory performance, relative to baseline, than peers who stayed awake for the same period.
5. Methods
5.1. Participants
Thirty-nine healthy adolescents (aged 15–18, 27 females) were recruited from a live-in, full time English-speaking boarding
school in Hong Kong. Participants signed up voluntarily with the Head of Boarding at the school after a recruitment presentation.
Participants were screened with a questionnaire and were excluded if they reported a: 1) sleep disorder, 2) significant medical
condition, 3) reading, writing or language disorder, and 4) visual or hearing impairment. Students' responses were reviewed by a
clinical psychology trainee (SM) supervised by a qualified clinical psychologist (EYYL). Students aged 18 were provided with written
informed consent, while consent for students under 18 was provided by the headmaster, who acted ‘in loco parentis’ for them. The
study was reviewed and approved by the Psychology Department Research Ethics Committee, The University of Hong Kong.
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E.Y.Y. Lau et al. Journal of Adolescence 67 (2018) 77–84
5.2. Procedures
For one week prior to the testing date, students were instructed to follow their habitual sleep-wake behaviors and to keep a sleep
diary to record their sleep onset time and wake-up time. The week was chosen as being representative of a normal week in terms of
sleep-wake schedule, as recommended by the Head of Boarding. Students were asked to avoid caffeinated beverages for 24 h prior to
the experiment to minimize the effects of caffeine on student's sleep the night prior to testing, and on performance on the day.
Previous research suggested that coffee consumed as far ahead as six hours before sleep may affect nocturnal sleep onset (Drake,
Roehrs, Shambroom, & Roth, 2013). Alcohol consumption was forbidden on as per school regulations.
Students were first matched for age, sex and sleepiness, using the Cleveland Adolescent Sleepiness Questionnaire (CASQ)
(Spilsbury, Drotar, Rosen, & Redline, 2007). They were then randomly assigned to either the nap (n = 20) or no-nap condition
(n = 19). Baseline assessment was scheduled at 2.00pm (Time 1; see Fig. 1 for the complete timeline), where students completed the
Stanford Sleepiness Scale (SSS). This, and all subsequent tasks, were administered to the group collectively in a classroom. After that,
students in the nap group were instructed to return to their rooms to take a nap. The nap opportunity was scheduled from 3.15pm to
4.15pm, a time period consistent with the post-lunch dip (Broughton, 1989). The one-hour nap opportunity was a duration com-
parable to previous napping studies (e.g. Lo et al., 2017; Morita et al., 2012; Tucker & Fishbein, 2008). Students in the no-nap group
were instructed to do solitary activities during the same period. Students in the nap group were instructed to end the nap at 4.15pm
using their usual alarm method, and then to report whether they fell asleep. The retest session was scheduled at 5.15pm (Time 2;
Fig. 1). Until the retest session students relaxed on their own. They were instructed not to exercise and not to use any memory
strategies in the period between baseline and retest sessions. At 5.15pm students were retested on the same tasks, except for List B in
the Word List task, which was used to measure new learning and was only presented at Time 2.
5.3. Measures
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E.Y.Y. Lau et al. Journal of Adolescence 67 (2018) 77–84
Table 1
Demographics of the sample.
Nap group (n = 16) No-nap group (n = 17) t/χ2 Cohen's d/W p
non-target words. At retest, students engaged in free recall of List A. Another 15-word list (List B) was then presented to measure new
learning. A recognition test of all 30 words from List A and B was then administered.
5.3.6. Word Pair Associates task (adapted from Tucker & Fishbein, 2008)
Forty semantically unrelated word pairs were read out with a 1-s interval between items (e.g. boat–phone). After all the word
pairs were presented, the first word of each word pair was presented as a cue for recalling the paired word. The same testing
procedure was repeated at retest. Prior to starting the task, students had been prompted to use any memory strategies they would
normally employ. Previous studies found this task to be sensitive in detecting sleep-related benefits in verbal associative memory
(Payne et al., 2012; Tucker & Fishbein, 2008).
Independent t-tests or chi-square tests were used to compare age, sex ratio, CASQ scores, and habitual sleep duration between the
nap and no-nap groups. 2 × 2 mixed design analyses of variance (ANOVAs) were conducted on memory tasks with a within-subject
factor (time: baseline vs. retest) and a between-subject factor (group: nap vs no-nap). For measures without a baseline score (i.e., List
B), between-group differences were tested with a one-way ANOVA.
6. Results
Four students of the nap group reported not sleeping during the napping opportunity, and two students of the no-nap group failed
to return for retest session. Data for these subjects were removed from all analyses. The final sample consisted of 33 participants in
total, with 24 females, n = 16 in nap group, overall mean age = 17.18 years (Table 1). The two groups did not significantly differ in
age, sex ratio, habitual sleep duration or habitual sleepiness. There was no group difference in baseline state sleepiness on SSS (t
(31) = −.908, p = .371). The mean score for SSS was 3.50 and 3.18 in the nap group and the no-nap group, respectively, suggesting
an alertness level of being “awake, but relaxed; responsive but not fully alert” (MacLean et al., 1992). Whilst not indicative of
excessive sleepiness in a clinical sense, the score suggests elevated sleepiness, particularly if the demands of the testing situation in
increasing arousal are taken into account.
There was a significant Time × Group interaction, F(1,29) = 12.80, p = .001, η2 = .31 (Table 2), such that the nap group de-
monstrated a significant decrease in sleepiness from baseline to retest, t(15) = 3.171, p = .006, while subjective sleepiness in the no-
Table 2
Group comparisons pre- and post-condition.
Nap group (n = 16) No-nap group (n = 17) Ftime Fgroup Ftimexgroup
SSS 3.50 (1.03) 2.44 (1.03) 3.18 (1.01) 3.73 (1.75) 1.407 1.615 12.800∗∗∗
Prose stories 17.78 (2.47) 16.72 (2.97) 17.00 (3.18) 14.78 (3.25) 36.434∗∗∗ 1.778 4.524∗
Word List A recall 11.50 (2.53) 10.00 (3.98) 12.18 (2.16) 9.76 (2.97) 17.291∗∗∗ .057 .939
Word List B learning N/A 12.06 (1.73) N/A 10.94 (2.79) N/A 1.891 N/A
Word Lists recognition 13.33 (2.47) 24.47 (4.21) 13.76 (1.39) 24.25 (3.86) 394.820*** .005 .273
Word Pair Associates 33.06 (9.33) 32.50 (9.80) 32.81 (6.82) 30.31 (8.01) 12.650∗∗∗ .165 5.063∗
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E.Y.Y. Lau et al. Journal of Adolescence 67 (2018) 77–84
Fig. 2. Performance in Prose Stories Recall task decreased in both nap and no-nap group but the effect was less pronounced in nap group.
nap group increased, although not at a level of significance t(14) = −1.835, p = .088.
Fig. 3. Performance in Word Pair Associates task decreased in both nap and no-nap group but the effect was less pronounced in nap group.
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7. Discussion
This was the first study to demonstrate the effects of napping with a field experiment in adolescents, a population that commonly
presents with inadequate sleep and daytime sleepiness. The benefit of a nap was evident despite uncontrolled, extraneous variables
which might affect sleep quality and duration in the sleeping quarters at a boarding school. Results highlighted the potential strategic
use of napping in supporting students' learning via ameliorating the negative consequences of inadequate sleep.
Consistent with the literature in adult samples (Tietzel & Lack, 2001), the current results suggested that napping could sig-
nificantly reduce subjective sleepiness in adolescents. A nap appears to have protected students from the decrement in alertness often
referred to as the “post-lunch dip”, a commonly observed circadian rhythm effect (Broughton, 1989). Given the previously de-
monstrated importance of self-reported sleepiness as a predictor of academic performance (Howell, Jahrig, & Powell, 2004; Shin,
Kim, Lee, Ahn, & Joo, 2003), our findings may have important implications for the potential use of napping as an intervention to
ameliorate daytime sleepiness in adolescents. Whilst the design of our study precluded us from informing on the effects of a dif-
ferently-timed nap intervention, the positive results support scheduling naps for adolescents after lunch. The timing of the nap
opportunity was designed to be maximally beneficial by coinciding with circadian body temperature changes and the “post-lunch
dip”. Napping is more natural at this time so it is likely that napping effects may be most marked when scheduled in the afternoon.
Also, as the maximum nap opportunity was one hour, research suggests it is unlikely to have a negative impact on sleep circadian
timing or to delay sleep onset later that night (Pilcher, Michalowski, & Carrigan, 2001). Indeed, this sleep lab's previous study in
undergraduate students found that a daytime nap opportunity of up to 90 min did not result in worse nighttime sleep behaviors when
compared to an equivalent period of wake (Lau et al., 2015). Taken together, the results suggest short naps represent a promising
strategy to alleviate daytime sleepiness and enhance learning without detrimental effects on night-time sleep nor the logistic chal-
lenge of starting schools later to accommodate teenage sleep-phase delay. Also of note, participants expressed positive views about
the incorporation of napping into their daily routines. Future research may wish to investigate the receptiveness of other stakeholders
to napping interventions at school.
Our results showed that a daytime nap opportunity of less than one hour had a protective effect on declarative memory, above an
equivalent period of wake. A unique feature of the present study was that all the tasks were administered verbally instead of being
presented on a screen or on paper. The current study found a similar effect of napping on declarative associative memory with
previous studies using visually presented tasks (Plihal & Born, 1997; Tucker et al., 2006). This finding is in line with the research of
Brand and Jolles (1985), who found no differential effect between presentation modes (i.e. auditorily and visually) on declarative
associative memory. Sleep seems to facilitate verbal memory regardless of the information processing modality. Interestingly, the nap
facilitated verbal memory in free recall (prose stories) and cued recall paradigms involving associative learning (Word Pair As-
sociates), but not on recognition memory tasks, which were item-based. This pattern is in line with previous findings that associative
learning and item-based learning are neuro-anatomically and functionally separable. According to one fMRI study (Davachi &
Wagner, 2002), the hippocampus was more engaged in the processing of associative learning, while item-based processing was
associated with greater activity in entorhinal and parahippocampal regions. As the hippocampus is more involved in associative
learning, our results seem to provide peripheral evidence that sleep-dependent memory consolidation involves the hippocampus and
may not occur when alternate brain structures are dominant as in item-based learning (Wagner, Kashyap, Diekelmann, & Born,
2007).
Our findings did not show a performance benefit in new learning between the nap and no-nap group. A previous study de-
monstrated that benefits to new learning only happened under a low sleep pressure condition and that benefits were positively
related to the amount of REM sleep achieved during naps (Cajochen et al., 2004). The one-hour nap opportunity in our design was not
long enough for REM sleep to emerge, despite the alleviation of sleep pressure.
7.3. Limitations
A major limitation of our naturalistic paradigm was that we did not have objective measures of sleep such as polysomnography or
actigraphy but relied solely on students' self-report of their sleep vs. wake. That said the incentive for participants to lie about falling
asleep in the nap group was low, and the majority of the participants (16 out of 20) reported to have napped. Also, any undeclared
napping in the no-nap group would have biased our results in favor of null findings, suggesting that the actual effects of napping
might have been even larger than those currently reported. In the present study, the actual length of the nap was not recorded or
reported, but it would be interesting for future studies to take into account the potential effects of the length of napping on memory
consolidation. Another limitation of this study was that we did not control the sleep environment of individual students. The potential
variability of the dormitory rooms and the surroundings might have introduced unknown extraneous factors between conditions.
Nevertheless, the living/sleeping conditions of each dormitory room were similar and we deemed the ecological validity of our
findings outweighed the costs on variability. Thirdly, the gender ratio of the study participants was biased towards females, which
may limit the generalizability of our findings to male students. Nevertheless, as reported by the Head of School, the school had a
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gender ratio bias of 6:4 (female vs. male) so it was more likely for females to be recruited in the study. Interestingly, previous studies
have reported heightened sleepiness in girls as compared to boys (Chung & Cheung, 2008; Ohayon, Roberts, Zulley, Smirne, & Priest,
2000). Results from this study support the significance and relevance of investigating the use of napping interventions with female
students. Fourthly, our study adopted group testing procedures, which is typical in school settings but limits the generalizability of
our findings to other testing situations. Future research may wish to consider individual testing and a longer experiment using a
within-subjects design which would further reduce measurement error. Lastly, it would be helpful to incorporate more detailed
habitual sleep data in future studies in order to investigate whether habitual circadian phase has an effect on the participant's
performance.
8. Conclusion
The findings suggested that a daytime nap opportunity supports consolidation of declarative memory among adolescents. To
alleviate the problem of inadequate sleep and sleep difficulties commonly found in adolescents in developed countries worldwide, the
incorporation of daytime napping in school schedules could be further explored, as evidence for the benefits of napping on learning
and memory consolidation and retention accumulates.
Disclosure
This study did not receive any financial support. The authors have no conflicts of interest.
Acknowledgement
Our gratitude goes to Li Po Chun, United World College, Hong Kong for its full support in data collection. We also thank the
anonymous reviewers and the editor for their constructive comments and suggestions for earlier versions of the manuscript.
References
Antonenko, D., Diekelmann, S., Olsen, C., Born, J., & Mölle, M. (2013). Napping to renew learning capacity: Enhanced encoding after stimulation of sleep slow
oscillations. European Journal of Neuroscience, 37, 1142–1151.
Brand, N., & Jolles, J. (1985). Learning and retrieval rate of words presented auditorily and visually. The Journal of General Psychology, 112, 201–210.
Broughton, R. J. (1989). Chronobiological aspects and models of sleep and napping. In D. Dinges, & R. Broughton (Eds.). Sleep and Alertness: Chronobiological ,
behavioural and medical aspects of napping. Raven Press.
Cajochen, C., Knoblauch, V., Wirz-Justice, A., Kräuchi, K., Graw, P., & Wallach, D. (2004). Circadian modulation of sequence learning under high and low sleep
pressure conditions. Behavioural Brain Research, 151(1), 167–176.
Chung, K., Chan, M., Lam, Y., Lai, C. S., & Yeung, W. (2017). School-based sleep education programs for short sleep duration in adolescents: A systematic review and
meta-analysis. Journal of School Health, 87, 401–408.
Chung, K., & Cheung, M. (2008). Sleep-wake patterns and sleep disturbance among Hong Kong Chinese adolescents. Sleep, 31, 185–194.
Davachi, L., & Wagner, A. D. (2002). Hippocampal contributions to episodic encoding: Insights from relational and item-based learning. Journal of Neurophysiology, 88,
982–990.
Drake, C., Roehrs, T., Shambroom, J., & Roth, T. (2013). Caffeine effects on sleep taken 0, 3, or 6 hours before going to bed. Journal of Clinical Sleep Medicine, 9, 1195.
Ellenbogen, J. M., Hulbert, J. C., Jiang, Y., & Stickgold, R. (2009). The sleeping Brain's influence on verbal Memory: Boosting resistance to interference. PLoS One, 4(1),
e4117.
Ellenbogen, J. M., Hulbert, J. C., Stickgold, R., Dinges, D. F., & Thompson-Schill, S. (2006). Interfering with theories of sleep and memory: Sleep, declarative memory,
and associative interference. Current Biology, 16, 1290–1294.
Fallone, G., Owens, J., & Deane, J. (2002). Sleepiness in children and adolescents: Clinical implications. Sleep Medicine Reviews, 6, 287–306.
Gibson, E., Powles, A., Thabane, L., O'Brien, S., Molnar, D., Trajanovic, N., ... Chilcott-Tanser, L. (2006). “Sleepiness” is serious in adolescence: Two surveys of 3235
Canadian students. BMC Public Health, 6, 116.
Gradisar, M., Gardner, G., & Dohnt, H. (2011). Recent worldwide sleep patterns and problems during adolescence: A review and meta-analysis of age, region and sleep.
Sleep Medicine, 12, 110–118. http://dx.doi.org/10.1016/j.sleep.2010.11.008.
Hirshkowitz, M., Whiton, K., Albert, S., Alessi, C., Bruni, O., Doncarlos, L., ... Ware, J. (2015). National Sleep Foundation's updated sleep duration recommendations:
Final report. Sleep Health, 1, 233–243.
Howell, A., Jahrig, J., & Powell, R. (2004). Sleep quality, sleep propensity and academic performance. Perceptual and Motor Skills, 99, 525–535.
Lau, E., Wong, M., Lau, K., Hui, F., & Tseng, C. (2015). Rapid-eye-movement-sleep (REM) associated enhancement of working memory performance after a daytime
nap. PLoS One, 10, e0125752.
Lim, J., Lo, J., & Chee, M. (2017). Assessing the benefits of napping and short rest breaks on processing speed in sleep‐restricted adolescents. Journal of Sleep Research,
26, 219–226.
Lo, J. C., Dijk, D. J., & Groeger, J. A. (2014). Comparing the effects of nocturnal sleep and daytime napping on declarative memory consolidation. PLoS One, 9(9),
e108100.
Lo, J. C., Groeger, J. A., Santhi, N., Arbon, E. L., Lazar, A. S., Hasan, S., ... Dijk, D. (2012). Effects of partial and acute total sleep deprivation on performance across
cognitive domains, individuals and circadian phase. PLoS One, 7(9), e45987.
Lo, J., Lee, S., Teo, L., Lim, J., Gooley, J., & Chee, M. (2017). Neurobehavioral impact of successive cycles of sleep restriction with and without naps in adolescents.
Sleep, 40(2), 1–9.
Lo, J. C., Ong, J. L., Leong, R. L., Gooley, J. J., & Chee, M. W. (2016). Cognitive performance, sleepiness, and mood in partially sleep deprived adolescents: The need for
sleep study. Sleep, 39, 687–698.
MacLean, A., Fekken, G., Saskin, P., & Knowles, J. (1992). Psychometric evaluation fo the standford sleepiness scale. Journal of Sleep Research, 1(1), 35–39.
Maquet, P. (2001). The role of sleep in learning and memory. Science (New York, N.Y.), 294, 1048–1052.
Morita, Y., Ogawa, K., & Uchida, S. (2012). The effect of a daytime 2-hour nap on complex motor skill learning. Sleep and Biological Rhythms, 10, 302–309.
Ohayon, M. M., Roberts, R. E., Zulley, J., Smirne, S., & Priest, R. G. (2000). Prevalence and patterns of problematic sleep among older adolescents. Journal of the
American Academy of Child & Adolescent Psychiatry, 39, 1549–1556.
Payne, J. D., Tucker, M. A., Ellenbogen, J. M., Wamsley, E. J., Walker, M. P., Schacter, D. L., et al. (2012). Memory for semantically related and unrelated declarative
information: The benefit of sleep, the cost of wake. PLoS One, 7(3), e33079.
83
E.Y.Y. Lau et al. Journal of Adolescence 67 (2018) 77–84
Pilcher, J., Michalowski, K., & Carrigan, R. (2001). The prevalence of daytime napping and its relationship to nighttime sleep. Behavioral Medicine, 27, 71–76.
Plihal, A. R., & Born, J. (1997). Effects of early and late nocturnal sleep on declarative and procedural memory. The Journal of Cognitive Neuroscience, 9, 534–547.
Rey, A. (1964). L’examen clinique en psychologie [The clinical psychological examination]. Paris: Presses Universitaires de France.
Ribeiro, S., Goyal, V., Mello, C. V., & Pavlides, C. (1999). Brain gene expression during REM sleep depends on prior waking experience. Learning & Memory, 6, 500–508.
Schoenberg, M., Dawson, K., Duff, K., Patton, D., Scott, J., & Adams, R. (2006). Test performance and classification statistics for the Rey Auditory Verbal Learning Test
in selected clinical samples. Archives of Clinical Neuropsychology, 21, 693–703.
Shin, C., Kim, J., Lee, S., Ahn, Y., & Joo, S. (2003). Sleep habits, excessive daytime sleepiness and school performance in high school students. Psychiatry and Clinical
Neurosciences, 57, 451–453.
Spilsbury, J., Drotar, D., Rosen, C., & Redline, S. (2007). The Cleveland adolescent sleepiness questionnaire: A new measure to assess excessive daytime sleepiness in
adolescents. Journal of Clinical Sleep Medicine, 3, 603–612.
Stickgold, R. (2005). Sleep-dependent memory consolidation. Nature, 437, 1272–1278.
Tagaya, H., Uchiyama, M., Ohida, T., Kamei, Y., Shibui, K., Ozaki, A., ... Takahashi, K. (2004). Sleep habits and factors associated with short sleep duration among
Japanese high-school students: A community study. Sleep and Biological Rhythms, 2, 57–64.
Tietzel, A., & Lack, L. (2001). The short-term benefits of brief and long naps following nocturnal sleep restriction. Sleep, 21, 293–300.
Tucker, M., & Fishbein, W. (2008). Enhancement of declarative memory performance following a daytime nap is contingent on strength of initial task acquisition.
Sleep, 31, 197–203.
Tucker, M., & Fishbein, W. (2009). The impact of sleep duration and subject intelligence on declarative and motor memory performance: How much is enough? Journal
of Sleep Research, 18, 304–312.
Tucker, M. A., Hirota, Y., Wamsley, E. J., Lau, H., Chaklader, A., & Fishbein, W. (2006). A daytime nap containing solely non-REM sleep enhances declarative but not
procedural memory. Neurobiology of Learning and Memory, 86, 241–247.
Wagner, U., Kashyap, N., Diekelmann, S., & Born, J. (2007). The impact of post-learning sleep vs. wakefulness on recognition memory for faces with different facial
expressions. Neurobiology of Learning and Memory, 87, 679–687.
Walker, M., & Stickgold, R. (2006). Sleep, memory, and plasticity. Annual Review of Psychology, 57, 139–166.
Walker, M. P., Stickgold, R., Jolesz, F. A., & Yoo, S. S. (2005). The functional anatomy of sleep-dependent visual skill learning. Cerebral Cortex, 15, 1666–1675. https://
doi.org/10.1093/cercor/bhi043.
Wechsler, D. (1997). WMS-III administration and scoring manual. San Antonio: Psychological Corporation.
Wolfson, A., & Carskadon, M. (1998). Sleep schedules and daytime functioning in adolescents. Child Development, 69, 875–887.
Wong, M., Lau, E., Wan, J., Cheung, S., Hui, C., & Mok, D. (2013). The interplay between sleep and mood in predicting academic functioning, physical health and
psychological health: A longitudinal study. Journal of Psychosomatic Research, 74, 271–277.
Woods, & Scott (2016). Sleepyteens: Social media use in adolescence is associated with poor sleep quality, anxiety, depression and low self-esteem. Journal of
Adolescence, 51, 41–49.
Yang, C., Kim, J., Patel, S., & Lee, J. (2005). Age-related changes in sleep/wake patterns among Korean teenagers. Pediatrics, 115, 250–256.
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