pii: sp- 00579-15 http://dx.doi.org/10.5665/sleep.

6092

SLEEP COGNITION AND BEHAVIOR

Sleep Restriction Impairs Vocabulary Learning when Adolescents Cram for

Exams: The Need for Sleep Study
Sha Huang, PhD1; Aadya Deshpande, BS1; Sing-Chen Yeo, BS1; June C. Lo, PhD1; Michael W.L. Chee, MBBS1; Joshua J. Gooley, PhD1,2
1
Center for Cognitive Neuroscience, Program in Neuroscience and Behavioral Disorders, Duke-NUS Medical School, Singapore; 2Department of Physiology, Yong Loo Lin
School of Medicine, National University of Singapore, Singapore

Study Objectives: The ability to recall facts is improved when learning takes place at spaced intervals, or when sleep follows shortly after learning. However,
many students cram for exams and trade sleep for other activities. The aim of this study was to examine the interaction of study spacing and time in bed (TIB)
for sleep on vocabulary learning in adolescents.
Methods: In the Need for Sleep Study, which used a parallel-group design, 56 adolescents aged 15–19 years were randomly assigned to a week of either 5
h or 9 h of TIB for sleep each night as part of a 14-day protocol conducted at a boarding school. During the sleep manipulation period, participants studied 40
Graduate Record Examination (GRE)-type English words using digital flashcards. Word pairs were presented over 4 consecutive days (spaced items), or all
at once during single study sessions (massed items), with total study time kept constant across conditions. Recall performance was examined 0 h, 24 h, and
120 h after all items were studied.
Results: For all retention intervals examined, recall of massed items was impaired by a greater amount in adolescents exposed to sleep restriction. In
contrast, cued recall performance on spaced items was similar between sleep groups.
Conclusions: Spaced learning conferred strong protection against the effects of sleep restriction on recall performance, whereas students who had
insufficient sleep were more likely to forget items studied over short time intervals. These findings in adolescents demonstrate the importance of combining
good study habits and good sleep habits to optimize learning outcomes.
Keywords: sleep, spaced learning, vocabulary learning, declarative memory, adolescents
Citation: Huang S, Deshpande A, Yeo SC, Lo JC, Chee MW, Gooley JJ. Sleep restriction impairs vocabulary learning when adolescents cram for exams: the
Need for Sleep Study. SLEEP 2016;39(9):1681–1690.

Significance
Many adolescents are exposed to sleep restriction during school days. This behavior could have negative consequences for learning of skills and
facts, hence eroding the value of formal education. Most research on the role of sleep in declarative memory has focused on recall performance after a
single study opportunity, while in real life students usually learn across days. We found that adolescents exposed to sleep restriction exhibited greater
forgetting of items that were learned during single study sessions, but not when items were studied over multiple days. Students with insufficient sleep
who cram for exams might be especially prone to forgetting newly learned material, but deficits in learning can be minimized by spacing study sessions
over time.

INTRODUCTION have been demonstrated for a wide variety of learning tasks

Many students are habitually exposed to sleep restriction ranging from fine motor skills to vocabulary learning, as-
during school days.1–4 In the United States, the majority of sessed either in the laboratory or in the classroom.12–15 In his
adolescents aged 15–17 years report sleeping 7 h or less per analyses of retention as a function of time, Ebbinghaus found
night,5 while the National Sleep Foundation recommends 8–10 that recall performance showed little drop-off between 9 h to
h of sleep for this age group.6 The high prevalence of sleep 24 h after learning (i.e., spanning the night), as compared to
restriction is alarming because deficits in learning and related retention assessed before and after this interval. His findings
cognitive faculties such as attention occur following insuffi- were later replicated and extended by others,16,17 demonstrating
cient sleep.7,8 Additionally, when sleep is sacrificed for other that retention is better if followed by sleep rather than wakeful-
late-night activities, test scores and performance on assign- ness.7,18 For decades, it was assumed that less forgetting occurs
ments on the following day generally suffer.9 Furthermore, across a night of sleep because there is less memory interfer-
many students procrastinate on studying for exams,10 which ence compared to the daytime.19 However, recent work sug-
can lead to cramming at the expense of sleep. Presumably, a gests that memories are actively strengthened and stabilized
more effective strategy for long-term learning would be to during sleep.20
space studying over multiple days with intervening episodes Despite the benefits of increased study spacing and sleep
of sufficient sleep. on memory, little is known about how these factors interact
More than 130 years ago, Hermann Ebbinghaus conducted to influence long-term learning. In a meta-analysis of spaced
a series of pioneering studies on learning and memory in learning on verbal memory tasks, it was shown that for reten-
which he described the basic properties of learning and forget- tion intervals ranging from a day to a month, the spacing ef-
ting curves.11 As part of this work, Ebbinghaus showed that fect was greatest when the interval between study sessions was
long-term retention is improved when studying takes place about a day.12 Because the focus of these studies was on the
at spaced intervals, as opposed to all at once. Hence, simply effects of study spacing, the potential role of sleep in learning
re-distributing study time can improve memory, even when was not considered. Recently, it was shown that long-term re-
total study time is kept constant. The advantages of increased tention of Swahili-English translations was better when sleep
study spacing for long-term learning (i.e., the spacing effect) occurred between evening and morning study sessions, as

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 compared to an equivalent period of wakefulness between Matrices for evaluating non-verbal intelligence.30 Individuals
morning and evening study sessions.21 These results indicate who completed the initial screening visit were required to wear
that sleep between encoding and restudying improves long- an actigraphy device (Actiwatch 2, Philips Respironics Mini-
term memory. However, it has yet to be examined whether re- Mitter, Bend, OR) on their non-dominant wrist for 1 week
peated exposure to sleep restriction, which often occurs during during their school term. Participants were excluded if they
the school week in adolescents, modulates the effects of study were habitual short sleepers, defined as having an average
spacing on memory. daily time in bed (TIB) < 6 h per night with less than 1 h of
The goal of the present study was to characterize the inter- sleep extension on weekends versus weekdays.
action between sleep duration and study spacing on long-term
vocabulary learning. We hypothesized that if sleep accounts Protocol Overview
for a large portion of the spacing effect, then individuals ex- Subjects took part in a 14-day study conducted at a boarding
posed to sleep restriction would show a smaller benefit of school in Singapore. In the week before the study, subjects
increased study spacing on long-term learning, as compared were required to maintain a fixed sleep-wake schedule with 9 h
to individuals with longer sleep. Alternatively, if exposure to of TIB per night from 23:00 to 08:00, which was verified by ac-
partial sleep deprivation leads to greater forgetting of items tigraphy monitoring. To accommodate study planning, partici-
that are studied only once rather than spaced across days, then pants were randomly assigned to 9-h TIB and 5-h TIB groups
increasing the degree of study spacing would result in a larger (n = 30 per group) prior to the start of the 14-day protocol;
benefit on vocabulary learning in individuals exposed to sleep however, they were not informed of their assignment until the
restriction. first day of the study. Of the 30 subjects who were assigned to
the 9-h TIB group, 2 subjects withdrew before the start of the
METHODS 14-day study, and 1 participant withdrew during the second
baseline day due to personal reasons. Another subject in the
Subjects and Recruitment 9-h TIB group completed the study but was excluded post
Healthy adolescents (n = 60) aged 15–19 years took part in hoc when it was determined that he did not comply with the
the Need for Sleep Study22 during their vacation period (No- sleep schedule. Therefore, the 9-h TIB group had 26 partici-
vember 26 to December 9, 2014). Most students were recruited pants (11 males, mean ± standard deviation [SD] = 16.8 ± 1.2
during open-invitation information sessions held at their re- years) and the 5-h TIB group had 30 participants (14 males,
spective schools, while others responded to advertisements or mean ± SD = 16.4 ± 0.9 years).
learned about the study through their peers. Interested students The 14-day protocol consisted of 3 nights of baseline sleep,
attended a study briefing session with at least one of their par- 7 nights of sleep manipulation, and 3 nights of recovery sleep
ents. Informed written consent was obtained from at least one (Figure 1). Subjects arrived at the boarding school in the
parent with assent provided by his/her child. Study procedures morning and were oriented to study procedures on the first day
were approved by the National University of Singapore Institu- of the protocol. During the baseline nights, all subjects were
tional Review Board, and research was compliant with ethical given a 9-h opportunity for sleep from 23:00 to 08:00. Over the
principles outlined in the Declaration of Helsinki. next 7 nights, students who were assigned to the 9-h TIB group
Potential subjects completed a series of questionnaires to kept the same sleep-wake schedule (Figure 1A), whereas the
determine their eligibility and health status. The Beck Anxiety 5-h TIB group was allowed to sleep from 01:00 to 06:00 each
Inventory was used to exclude individuals with moderate to night (Figure 1B). On the final 3 nights of the study, all partici-
severe anxiety levels (score ≥ 16),23 and the Beck Depression pants were given a 9-h sleep opportunity from 23:00 to 08:00.
Inventory II was used to exclude participants with moderate Subjects were discharged from the study on the following day.
to severe depressive symptoms (score ≥ 20).24 Subjects were
ineligible if they had a history of psychiatric illness, central Study Environment
nervous system disease, or organ disease (e.g., renal or liver The study took place at the boarding school while school was
impairment). Participants underwent a face-to-face interview out of session, and hence the facilities described here were
to ascertain that they would be comfortable living with rela- used primarily by study participants. Subjects remained on
tive strangers in a community setting for a 2-week period. site for the full 2 weeks, and were under constant supervision
Additional exclusionary criteria included high risk for sleep by the researchers. During their free time, students spent most
apnea assessed using the Berlin Questionnaire,25 a body mass of their time in a large common room that had both natural
index ≥ 30 kg/m2, travel across more than 2 time zones in the and electric lighting. They were permitted to play games, read,
month before the study, or consumption of ≥ 5 caffeinated bev- review school work, and use their personal electronic devices
erages per day. Subjects also completed several questionnaires for entertainment. Subjects were also allowed to interact freely
that were not used to determine eligibility, including the Pitts- with other study participants and research staff members. Nap-
burgh Sleep Quality Index to assess sleep quality in the past ping, caffeinated beverages, and strenuous physical activity
month26; the Horne-Östberg Morningness-Eveningness Ques- were prohibited. Subjects were served breakfast, lunch, and
tionnaire to determine chronotype27; the Epworth Sleepiness dinner in a school cafeteria, and had free access to snacks
Scale to assess excessive daytime sleepiness28; the Chronic during their free time in the common room.
Sleep Reduction Questionnaire for measuring symptoms of On each day of the study, participants completed a com-
chronic sleep restriction29; and Raven’s Advanced Progressive puter-based neurobehavioral test battery (~30 min) in the

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 morning, afternoon, and evening (10:00,
15:00, and 20:00), as described in our pre-
vious work.22 Several stand-alone tests
were also administered during the course
of the study, including the vocabulary
learning task described here. All testing
took place in a standard classroom setting
with assigned seating. A study laptop was
assigned to each student, which allowed
all subjects to complete tests at the same
time.
At night, students slept in separate beds
in a residence building with 2 students
per room. Each room was air-conditioned
and had an attached bathroom. Male and
female students were housed in different
residential blocks, and the different sleep
groups (9 h TIB and 5 h TIB) were housed
on different floors. The windows in each
bedroom were covered by the investigators
to minimize the amount of sunlight in the
morning. Subjects were also provided with
ear plugs to reduce noise and were allowed
to adjust the temperature of their rooms.
Polysomnographic data were analyzed on
selected nights of the study (nights 3, 4, 7,
10, 11, and 13) to validate the sleep manip-
ulation. As reported elsewhere, both sleep
Figure 1—Sleep schedule and flashcard spacing. Adolescents took part in a 14-day research
groups slept a similar amount at baseline,
study carried out at a boarding school. After 3 baseline nights with 9 h of time in bed (TIB) for
whereas the 5-h TIB condition was associ- sleep, participants were exposed to 7 nights with either (A) 9 h of TIB from 23:00 to 08:00, or (B)
ated with a large daily reduction in total 5 h of TIB from 01:00 to 06:00, followed by 3 recovery nights with 9 h of TIB for sleep. Over a
sleep time relative to the 9-h TIB condi- period of 4 consecutive days (days 4–7), students completed a vocabulary learning task in which
tion.22,31 Bedtimes and wake times were they studied 40 Graduate Record Examination (GRE)-type words. Cued recall tests were given
enforced by researchers who stayed in the immediately after each study session, and also 24 h and 120 h after studying (days 8 and 12).
residence halls, and students were asked to After the test given on day 12, students were given a one-time review session that was followed
surrender their personal electronic devices by another cued recall test. In panels A and B, S = study sessions; CR = cued recall tests; and
during sleep periods. R = review. (C) For each participant, flashcards were randomly partitioned into a stack of 20 cards
shown twice per day across each of the study sessions (spaced items), and 4 smaller stacks with
a different set of cards shown each day (massed items). Spaced items and massed items were
Vocabulary Learning Task and Study presented in different blocks, with the order of presentation randomized and counterbalanced in
Spacing each sleep group. Panel C is modified from Kornell, Applied Cognitive Psychology, 2009.32
Subjects were oriented to the vocabulary
learning task on the fourth day of the study
(i.e., after the last baseline night), with instructions given to Subjects were instructed that they would be tested later on a
all participants at the same time. Studying and testing oc- cued recall test, during which they would have to report the
curred in the same classroom with assigned seating, and lap- matching word for each of the 40 cue words. During study ses-
tops were used to administer the task. Participants were made sions, the “front” of each flashcard (the cue word) was shown
fully aware of the study and testing schedule at the start of for 5 seconds (e.g., encomium:_____), followed by the “back”
the experiment. The vocabulary learning task took place at of the flashcard (the target word) for another 5 seconds (e.g.,
13:45 each day over 4 consecutive days (days 4 to 7). Across ______:praise). This was followed immediately by presenta-
the 4 study sessions, subjects studied 40 word pairs using tion of the next word pair. Digital flashcards were presented
digital flashcards (Figure 1C). Each word pair consisted of a using E-Prime 2.0 Professional software (Psychology Soft-
Graduate Record Examination (GRE)-type English word (the ware Tools, Inc, Sharpsburg, PA).
cue word) followed by a synonym (the target word). We chose Study spacing was manipulated by using flashcard stacks
to use GRE-type words, rather than unrelated word pairs, to of different sizes. All subjects were exposed to spaced and
ensure better ecological validity. The flashcard learning para- massed study conditions, with the order of presentation ran-
digm was based on a previous study that used the same set domly assigned and counterbalanced within each sleep group
of word pairs, which were selected because they represent the (9 h TIB and 5 h TIB). In each subject, the 40 word pairs were
types of words given on standardized tests such as the GRE.32 randomly partitioned into one stack of 20 flashcards (spaced

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 items) and 4 smaller stacks of 5 flashcards each (massed items) general characteristics of the learning curves. For data col-
(Figure 1C). Once the order of words within a flashcard stack lected during the retention and review phases of the study,
was assigned, it remained fixed for a given participant. Spaced statistical comparisons were performed using ANOVA with
items were presented twice during each of the 4 study sessions, 4 factors including TIB (9 h versus 5 h), flashcard spacing
whereas massed items were studied 8 times during a single (spaced versus massed), order of spacing (spaced first versus
session, with a new stack of 5 flashcards presented each day. massed first), and session/day of testing. TIB and order of
Therefore, subjects studied 25 flashcards per day, comprising spacing were between-subjects factors, and test session and
20 spaced items and 5 massed items (Figure 1C). By the end of flashcard spacing were within-subjects factors. We anticipated
the fourth study session, all word pairs were presented 8 times, that these factors might interact in complex ways to affect cued
with 80 seconds of total viewing time for each flashcard (40 recall performance. Because we did not have a strong theoret-
seconds each for the front and back). ical basis for including some interactions and dropping others
from the model, all possible interaction terms were considered
Cued Recall Test in the ANOVA. Analyses were performed using the general-
During cued recall tests, participants were shown all 40 cue ized linear model function command in R version 3.1.1,34 with
words in random order. Each cue word was displayed for a fixed a Gaussian distribution and identity link function. Model pa-
period of 15 seconds, during which subjects were instructed to rameters were determined by maximum likelihood estimation,
type the target word beneath the cue word using their laptop and deviance was computed to measure how closely the pre-
keyboard. Tests were given immediately after each of the study dicted values from the fitted model matched the actual data.
sessions to track vocabulary learning (days 4–7). The rationale The significance of each main/interaction effect was assessed
for testing all 40 GRE-type cue words, even when subjects had by comparing the deviance for the full model with the devi-
yet to be exposed to every flashcard, was to evaluate whether ance for the reduced model (i.e., the nested model) with that
participants were able to guess the target words based on their particular effect removed. Because the sampling distribution
pre-existing knowledge. In addition to assessing recall imme- of deviance can be approximated by a χ 2 distribution, statis-
diately after each study session, cued recall tests were given tical comparisons between models were performed using a
24 h and 120 h after the final study session (days 8 and 12). Di- likelihood ratio χ 2 test (LR χ 2 ). Multiple comparison testing
rectly after the test that occurred at the 120-h retention interval, was performed using a Tukey Honestly Significant Difference
subjects were given a one-time review session in which all 40 test at a family-wise confidence level of 95%, and effect size
flashcards were shown once in random order. Similar to study was measured using eta-squared (η 2 ) (R version 3.1.1).
sessions, the front and back of each flashcard were shown for 5
seconds each. The review session was followed by a final cued RESULTS
recall test to evaluate the benefit of the review session on recall Subjects who were assigned to the 9-h and 5-h TIB groups
performance. were similar for all measures taken during the screening pro-
cess, including basic subject characteristics, sleep behavior,
Analyses and Statistics anxiety and depression scores, and nonverbal intelligence
For each of the cued recall tests, responses were analyzed (Table 1). Based on actigraphy-estimated sleep duration during
using an algorithm that counted both correctly spelled an- the school term, subjects assigned to both sleep groups slept
swers and misspelled correct answers as correct responses about 2 h more on weekends versus school days. After a
(Lenient scorer program, N. Kornell).33 The score on each test 1-week washout period during the school holiday period with
was converted to a percentage (correct responses/number of a prescribed 9-h sleep schedule (23:00 to 08:00), students par-
tested items × 100%) prior to performing statistical analyses. ticipated in the 14-day study at the boarding school. Effects of
Test scores were analyzed separately for the 3 different phases sleep duration and study spacing (spaced versus massed) on
of the experiment: study, retention, and review. Performance learning of GRE-type words were examined by exposing ado-
during the study phase was evaluated using cued recall tests lescents to a week of sleep restriction (5 h TIB) or an age-ap-
that were given immediately after each of the 4 study sessions propriate amount of sleep (9 h TIB) after each night of studying
(days 4–7). Retention was evaluated after all 40 flashcards had (Figure 1).
been studied, but without additional review, corresponding to First, we examined learning curves based on cued recall per-
tests that occurred immediately after the fourth study session formance on all 40 items tested immediately after each of the
(0 h, day 7), on the following day (24 h, day 8), and 5 days 4 study sessions that occurred on consecutive days. Both sleep
after the last study session (120 h, day 12). Finally, the benefit groups showed a nonlinear increase in recall performance for
of reviewing the flashcards was evaluated by comparing test spaced items across the 4 study sessions (Figure 2A), with the
scores before and after the one-time review session that oc- largest improvement observed between the first and second
curred 120 h after the last study session. study sessions. There was an approximately linear increase in
During the study phase, statistical comparisons were not test scores for massed items because participants were shown
performed for spacing effects because the number of spaced 5 new massed word pairs each day but were tested on all items
items and massed items differed during the first 3 study ses- from the beginning of the experiment. Because subjects were
sions, and were equal only after the fourth study session. We tested on some massed items on days 4–6 (study sessions 1–3)
therefore provide only descriptive results for the effects of that had not been encoded yet, we performed a secondary
study spacing during the study phase of the experiment, e.g., analysis which only involved test scores on those massed items

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 Table 1—Subject characteristics.
9h TIB (n = 26) 5h TIB (n = 30)
Measure Mean SD Mean SD t /χ 2 P
Age (years) 16.81 1.17 16.43 0.94 1.33 0.19
Sex (% males) 42.30 – 46.70 – 0.11 0.74
BMI (kg/m2) 20.38 2.55 20.43 2.88 0.07 0.94
BAI score 6.58 4.83 7.80 6.45 0.79 0.43
BDI score 5.19 4.68 6.90 5.49 1.24 0.22
RAPM score 10.38 1.06 9.77 1.98 1.43 0.16
ESS score 6.19 3.57 7.77 3.59 1.64 0.11
MEQ score 49.96 7.15 47.90 7.43 1.05 0.30
CSRQ score 33.81 5.13 34.50 5.77 0.47 0.64
PSQI score 4.58 2.58 5.17 2.32 0.90 0.37
Weekday TST (h) 5.37 0.73 5.61 0.86 1.11 0.27
Weekend TST (h) 7.53 1.14 7.46 1.10 0.21 0.84

TIB, time in bed for sleep; BMI, body mass index; BAI, Beck Anxiety Inventory; BDI, Beck Depression Inventory II; RAPM, Raven’s Advanced Progressive
Matrices; ESS, Epworth Sleepiness Scale; MEQ, Horne-Östberg Morningness-Eveningness Questionnaire; CSRQ, Chronic Sleep Reduction Questionnaire;
PSQI, Pittsburgh Sleep Quality Index; TST, total sleep time, estimated using actigraphy devices when school was in session; SD, standard deviation.

Figure 2—Vocabulary learning and cued recall performance in response to sleep restriction. (A) Learning curves for recall of spaced items and massed
items (20 items per condition) are shown for groups of adolescents exposed to either 9 h of time in bed (TIB) or 5 h of TIB for sleep after each day of learning.
Students were tested immediately after each study session. For items that were massed, test scores are shown separately for those items that had already
been studied (black traces), and for all 20 cue words (red traces) including those items that had yet to be encoded. (B) After spaced items and massed items
were studied an equal number of times, there was a significant interaction between study spacing and TIB (LR χ 2 = 8.40, P < 0.01), whereby sleep restriction
was associated with a significant decrease in cued recall performance on massed items (indicated by the red asterisk, P < 0.05), but not on spaced items.
(C) Following a review session on day 12 in which students were shown all word pairs one more time, a final cued recall test was administered (day 12*)
in which test scores on massed items improved substantially. The mean ± SEM is shown for performance on each cued recall test. Additional statistical
comparisons during the retention phase and review phase are summarized in Table 2 and in the main text.

that had been studied prior to testing (Figure 2A). By the end of forgetting (Figure 2B). There was a significant interaction
of the second study session, test performance was qualitatively between study spacing and TIB for sleep (Table 2), such that
similar on spaced items versus massed items, even though sub- test performance on massed items was poorer in individuals
jects had to remember twice as many spaced items with only who underwent sleep restriction (Tukey test, P < 0.001), while
half the number of flashcard presentations (20 spaced items test performance on spaced items was similar between sleep
shown 4 times each versus 10 massed items shown 8 times groups (Tukey test, P = 0.80; Figure 2B). Consequently, indi-
each). As expected, test scores for massed items and spaced viduals exposed to sleep restriction exhibited a larger improve-
items (20 per condition) were most similar by the end of the ment in test scores with increased study spacing (Figure 3A).
fourth study session, after all items had been studied an equal The magnitude of the spacing effect, defined as the differ-
number of times. ence in test scores for each participant on spaced items versus
Next, we evaluated cued recall performance across different massed items, was about 2-fold greater in individuals exposed
retention intervals (0 h, 24 h, and 120 h). Despite being exposed to sleep restriction (Figure 3B). Although there was a main
to an additional 4 days of either 9 h of TIB or 5 h of TIB after effect of order on test scores with better recall of items pre-
the final study session, neither sleep group showed evidence sented in the second study block of each study session, there

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 Table 2—Statistical summary of factors affecting cued recall performance.
Retention Phase Review Phase
Factor LR χ 2
P η 2
LR χ 2
P η2
Spacing 61.65 < 0.001* 0.150 21.28 < 0.001* 0.077
TIB 17.29 < 0.001* 0.041 7.55 < 0.01* 0.027
Session 3.19 0.20 0.008 14.67 < 0.001* 0.053
Order 14.96 < 0.001* 0.035 8.75 < 0.01* 0.031
Spacing × TIB 8.40 < 0.01* 0.020 5.06 0.025* 0.018
Spacing × Session 1.30 0.52 0.003 6.85 < 0.01* 0.025
Spacing × Order 3.02 0.083 0.007 3.37 0.066 0.012
TIB × Session 0.092 0.96 < 0.001 1.53 0.22 0.006
TIB × Order 0.064 0.80 < 0.001 0.066 0.80 < 0.001
Session × Order 0.065 0.97 < 0.001 0.60 0.44 0.002

As part of a 14-day protocol, adolescents studied Graduate Record Examination (GRE)-type words over 4 consecutive days, and cued recall performance
was tested across different retention intervals (0 h, 24 h, and 120 h; days 7, 8, and 12 of the protocol), and before and after a vocabulary review (120 h;
day 12 of the protocol). For each phase of the experiment, a generalized linear model (GLM) was used to examine effects of study spacing (spaced versus
massed), time in bed (TIB) for sleep (9 h versus 5 h), test session, and order of study blocks (massed items first versus spaced items first) on cued recall
performance. Spacing and Session were within-subjects factors, and TIB and Order were between-subjects factors. All possible interactions were included
in the GLM. For each effect, the likelihood ratio χ 2 (LR χ 2) statistic was used to evaluate whether the goodness-of-fit for the reduced model (i.e., with that
effect removed) differed significantly from the full model with all predictor variables included. Results are shown for main effects and 2-way interactions.
All 3-way interactions and the 4-way interaction did not reach statistical significance (Retention phase: LR χ 2 ≤ 0.20, P > 0.8; Review phase: LR χ 2 < 1.3,
P > 0.2 for all 3-way/4-way interactions). Asterisks (*) indicate significant effects (P < 0.05), and effect sizes were estimated by eta-squared (η 2).

was no significant interaction involving order and other predic- There was a main effect of Session (LR χ 2 = 41.1, P < 0.0001,
tors (Table 2). Likewise, all 3-way interactions and the 4-way η 2 = 0.081) in which participants showed a drop in test scores
interaction did not reach statistical significance (LR χ 2 ≤ 0.20, from immediate recall to 24 h after the respective massed
P > 0.8 for all 3-way/4-way interactions). items were studied (e.g. from day 4 to day 5 for set 1, and
After a one-time review session in which subjects were given from day 5 to day 6 for set 2; Figure 4). Next, we conducted
an opportunity to study all 40 flashcards one more time, there a separate ANOVA to examine recall performance for dif-
remained a significant interaction between study spacing and ferent sets of massed items during the retention phase of the
TIB in which recall performance for massed items was worse experiment, i.e., 0 h, 24 h, and 120 h after all flashcard items
in individuals exposed to 5 h of TIB versus 9 h of TIB (Tukey were studied. There was a significant interaction between Set
test, P < 0.01), while test scores were similar between sleep and TIB (LR χ 2 = 10.71, P = 0.013, η 2 = 0.014); recall of the
groups for spaced items (Tukey test, P = 0.99). Additionally, first set of massed items was similar for the 9h TIB and 5h
there was a significant interaction between study spacing and TIB groups (Tukey test, P > 0.99), whereas participants who
test session (Table 2), whereby recall performance on massed underwent sleep restriction had lower test scores for massed
items improved after the review session, reaching a similar items that were presented on the second and third study ses-
level as for spaced items (Tukey test, P = 0.51) (Figure 2C). All sions (Set 2: Tukey test, P < 0.01 and Set 3: P < 0.001). Al-
3-way and 4-way interaction effects were not significant (LR though the difference in test scores between sleep groups did
χ 2 < 1.3, P > 0.2 for all interactions). not reach statistical significance for massed items presented
Because cued recall performance was different between during the fourth study session (Set 4: Tukey test, P = 0.15),
sleep groups only for the massed study condition, we con- the overall time-course of recall performance was compa-
ducted an exploratory analysis to assess whether testing per- rable to massed items presented on the second and third study
formance differed for massed items presented during each sessions (Figure 4).
of the different study sessions (Figure 4). First, we evaluated
whether overnight forgetting differed between sleep groups DISCUSSION
during the study phase for different sets of massed items. Our results show that daily exposure to partial sleep depri-
Based on an ANOVA with the factors Set (massed set 1, 2, 3, vation impaired vocabulary learning when studied word
and 4), Session (immediate versus 24 h later after a night of pairs were massed rather than spaced across consecutive
sleep), and TIB (9 h versus 5 h), there was a significant interac- days. Spaced learning conferred strong resistance to the ef-
tion between Set and TIB (LR χ 2 = 8.48, P = 0.037, η 2 = 0.017), fects of sleep restriction on memory, such that cued recall
such that the difference in recall performance between sleep performance was similar in students exposed to 9 h of TIB
groups was marginally greater for massed items presented in versus 5 h of TIB. Our results demonstrate that students ex-
Set 3 (Tukey test, P = 0.024) relative to Sets 1, 2, and 4. Ses- posed to sleep restriction can minimize the negative effects
sion did not interact with TIB (χ 2 = 1.70, P = 0.19), however, of sleep insufficiency on vocabulary learning by increasing
and no other interactions reached statistical significance. their study spacing.

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 Sleep Duration Modulates Effects of Study Spacing on Learning
Prior work has shown that memories can be strengthened by
increasing the spacing between study sessions, or by allot-
ting oneself adequate sleep. Our data extend these findings
by showing that study spacing and sleep duration interact to
influence vocabulary recall. The negative impact of sleep re-
striction on cued recall performance was greater for items that
were presented in the massed condition. This could be related
to decrements in attention and effort during encoding and re-
trieval. In the same group of students, we found that exposure
to sleep restriction resulted in a greater number of attentional
failures on a visual reaction time test.22 Because students were
presented with a greater number of repetitions for massed
items during each study session compared with spaced items,
attention and effort to study massed items might have dimin-
ished by a greater amount in sleep-restricted individuals once
these items became highly familiar,35,36 especially if students
thought that they had already mastered the material.37 In ad-
dition, exposure to 5 h of TIB might have impaired overnight
consolidation of massed items, as there was a trend for de-
creased recall performance on the day after encoding relative
to students given 9 h of TIB (Figure 4).
Almost all prior research on sleep-dependent learning and
consolidation of verbal memory has examined recall perfor-
mance after a single study session, even though this is not how
students learn ordinarily.38 In contrast to our results for massed
items that were studied this way, we found that sleep restriction
had no measurable effect on cued recall performance for items
that were spaced across 4 consecutive days, despite a 28-h re-
duction in the opportunity for sleep in the 5-h TIB condition
from the first day of studying to the final day of testing. The
protective effect of spaced studying during sleep loss could
be explained by the benefit of increased retrieval difficulty on
declarative memory. When items are studied only once (i.e.,
massed), exposure to insufficient sleep would be expected to
reduce encoding efficiency and increase retrieval difficulty,
resulting in poorer recall. However, when studying is spaced
Figure 3—Effects of study spacing on vocabulary learning were greater
out over time, increased retrieval difficulty at encoding may
during sleep restriction. Cued recall performance for Graduate Record
lead to strengthening of memory traces when these items are
Examination (GRE)-type words was examined across different retention
restudied, thus facilitating subsequent recall.39–42 This mecha- intervals for students who were given either 9 h of time in bed (TIB)
nism could serve to protect against the otherwise impairing for sleep each night, or 5 h of TIB. (A) The spacing effect, defined as
effects of sleep loss on learning and memory consolidation. the difference in test scores for spaced items versus massed items, is
It is also possible that the protective effect of increased study shown for each student across different retention intervals. In the heat
spacing is explained in part by increased contextual variability map, blue indicates better cued recall performance on spaced items,
at the time of encoding when items are spaced rather than and red indicates higher test scores on massed items. Cued recall
massed, leading to more cues available to aid in recall.43 performance was assessed immediately after the last study session,
and also 24 h and 120 h after all items were shown. This was followed
Interestingly, memory of massed items shown on the first
by a review session in which students were shown all word pairs once,
day of studying was similar between sleep groups, whereas
after which students were given a final cued recall test (120*h). (B) The
sleep restriction was associated with greater forgetting of magnitude of the spacing effect was greater in students given 5 h of TIB
massed items presented during other study sessions (Figure 4). versus 9 h of TIB (Spacing × TIB: LR χ 2 = 8.40, P < 0.01; See Table 2).
Because both sleep groups were given 9 h of TIB on the night The mean ± SEM is shown. The individual data in Panel A are aligned
before the first study session, the strength of encoding would be with group-averaged data in Panel B.
expected to be similar for the first set of massed items. By com-
parison, sleep loss on subsequent nights might have resulted in
weaker encoding of short-term memory,44 even if participants a critical threshold affecting sleep-dependent memory consoli-
were able to perform well on the immediate recall test, thus dation, whereas students were able to tolerate the first night
increasing the likelihood of forgetting of these items. Alterna- of partial sleep loss without detectable memory impairment.45
tively, it is possible that 2 nights of sleep restriction represented Although not tested in the present study, sleep might have

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 Figure 4—Sleep restriction impaired recall of massed items. Students who were exposed to either 9 h of time in bed (TIB) or 5 h of TIB for sleep used
digital flashcards to study Graduate Record Examination (GRE)-type words on 4 consecutive days (i.e., the study phase of the experiment, indicated by
the gray boxes). In the massed study condition, a different set of 5 word pairs was presented on each day (Set 1 – day 4; Set 2 – day 5; Set 3 – day 6;
Set 4 – day 7) and studied only once, with 8 repetitions per flashcard. For the first set of massed items that was studied, the time course of cued recall
performance was similar between sleep groups. In contrast, test scores for massed items shown during the other study sessions were consistently worse
in adolescents exposed to sleep restriction. There was a significant interaction between Set and TIB (LR χ 2 = 10.71, P = 0.013), in which students who were
exposed to sleep restriction showed significantly lower test scores for massed items presented in Sets 2 and 3 after all items had been studied (indicated
by red asterisks, P < 0.05). Additional statistical comparisons are presented in the main text. For each set of massed items, “S” indicates recall performance
immediately after each set of items was studied. The mean ± SEM is shown for performance on each cued recall test.

contributed differentially to the initial consolidation and later results for experiments in which encoding is either preceded
refinement of memory as participants were exposed to spaced by sleep restriction and followed by normal sleep, or preceded
items over the course of 4 consecutive days. For example, it has by normal sleep and followed by exposure to sleep restriction.
been shown that as a person masters a complex procedural task By comparison, our subjects were exposed to partial sleep de-
that requires training across multiple days (the Tower of Hanoi privation both before and after encoding of vocabulary items.
task), changes in EEG-derived sleep features associate with Additionally, the number of massed word pairs learned and the
improvements from initial training to mastery of the skill.46 At amount of sleep deprivation increased across study sessions.
present, however, it remains unclear whether sleep contributes Although this study design simulates what often occurs in ado-
to day-to-day improvements in declarative memory consolida- lescents during a typical school week, in which sleep depri-
tion beyond the first night after encoding. vation accumulates over multiple days, we cannot determine
Based on prior work on forgetting curves, we expected that with certainty which specific memory processes were affected
our participants would show a decrease in cued recall perfor- by exposure to sleep restriction.
mance as the lag between studying and testing was increased. We found that the spacing effect was nearly 2-fold greater
Contrary to our expectations, after the last study session there in the group of students exposed to sleep restriction, but the
was no evidence of forgetting in either sleep group for retention magnitude of the spacing effect likely depends on numerous
intervals up to 5 days after learning. The difference in cued factors, including the number and difficulty of items studied,
recall performance between the 5-h TIB and 9-h TIB groups the number of repetitions for each item, the degree of spacing
persisted until the one-time review session that occurred 120 h between items during a given study session (determined by the
after learning, which then boosted recall for massed items. Our size of the flashcard stack), the time duration between study
finding that exposure to 5 h of TIB did not result in greater sessions, and the length of the retention interval. Since only one
forgetting after all items had been studied is consistent with combination of these factors was examined, the spacing effect
prior work in adolescents demonstrating that recall of word might differ if any one of these parameters is manipulated. The
pairs learned prior to sleep restriction was intact.47 However, limited benefit of increased study spacing in the group of par-
it is possible that the lack of forgetting in our study could be ticipants given 9 h of TIB could also be explained in part by a
attributed to students learning the word pairs too well for a ceiling effect, since these students performed well at recalling
decrease in cued recall performance to be observed in the time items that were massed and had less room for improvement
window examined. This possibility could be addressed in fu- relative to the group that underwent sleep restriction. Addi-
ture studies by increasing the difficulty of the task, e.g., by in- tionally, recall performance on spaced items was very high for
creasing the number of word pairs, or by reducing the number both sleep groups, suggesting that these items might have been
of study sessions or number of times that the flashcards are over-studied. This might have prevented us from detecting
shown. deficits in recall for spaced items in the group of adolescents
exposed to 5 h of TIB that would otherwise be observed if the
Study Limitations and Considerations task was made more difficult. Another limitation of our study
The present study was not designed to tease apart the differen- is that we did not perform an a priori power analysis to assess
tial effects of sleep restriction on encoding versus memory con- whether our sample size would be adequate for the statistical
solidation. To examine this, it would be necessary to compare comparisons that were performed. It is therefore possible that

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 our sample size was insufficient for detecting differences in students choose to spontaneously cut large flashcard decks into
test scores for some of the variables and interactions that were smaller stacks,50 even though such behavior likely represents a
examined. suboptimal strategy for long-term learning.32 Moreover, when
To examine the effects of study spacing on a per individual asked to predict their recall performance of studied items that
basis, all students were exposed to massed items and spaced were massed or spaced, students often misjudge cramming as
items in separate blocks. Consistent with prior work, an order the better study strategy, even when their test results show the
effect was observed (Table 2), such that word pairs were better opposite effect.32
learned when presented in the second study block.32 In our As suggested in the present study, vocabulary learning is
study design, the order of massed items and spaced items was especially impaired when poor study strategies are combined
counterbalanced, and effects of order were taken into account with insufficient sleep. There are many factors contributing to
in the statistical analyses. The order of presentation did not chronic sleep loss in adolescents including early school start
interact with study spacing (Table 2), indicating that our find- times, caffeine consumption in the evening, late-night elec-
ings for TIB and study spacing were not confounded by order tronic media use, and school workload.51 These factors often
effects. lead to a disparity between sleep behavior on weekdays versus
In our study, participants were shown all 40 cue words weekends, and hence social and biological time, which has
during each cued recall test, including the study phase of the been dubbed “social jet lag.”3 Similar to the effects of rapid
experiment during which subjects were given 5 new massed travel across time zones, social jet jag and sleep debt can re-
items to study per day. Therefore, participants were tested on sult in fatigue and suboptimal performance. This potentially
items after each of the first 3 study sessions that had yet to be leads to poorer academic outcomes,52 with negative implica-
encoded. Although this allowed us to examine whether stu- tions for long-term learning. In students who habitually sleep
dents were able to guess target words before they were studied, less on school days versus free days, we show that exposure
we do not know whether advanced exposure to unpaired cue to sleep restriction reduces flashcard learning of GRE-type
words affected subsequent learning and recall of these massed words when studying is not spaced out over time. These re-
items. Upon close inspection of cued recall performance for sults indicate that cramming for exams and trading sleep for
massed items (Figure 4), it can be seen that test scores im- other activities may come at the expense of increased forget-
proved across study sessions by a small but consistent amount, ting, whereas increasing study spacing can serve to minimize
even for items that had yet to be studied. After an initial drop the negative effects of sleep loss on learning.
in recall performance on the day after each set of massed items
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