The power of children’s sleep - Improved declarative memory consolidation in children compared with adults

Abstract

Post-learning slow wave sleep (SWS) is known to support declarative memory consolidation. As SWS is more abundant in young population, we suggested that sleep-dependent memory consolidation processes could occur at a faster pace in school-aged children. After learning new associations between non-objects and their functions, retrieval performance was tested in 30 children (7–12 years) and 34 adults (20–30 years) during an immediate (IR) and a delayed retrieval (DR) session separated by either a Sleep or a Wake condition. Sleep led to stabilized memory retrieval performance only in children, not in adults, whereas no age-related difference was observed after a similar period of wakefulness. Hence, our results suggest more efficient sleep-dependent declarative memory consolidation processes in children compared with adults, an effect potentially ascribed to more abundant and deeper SWS during childhood.

Full text

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The power of children’s sleep -
Improved declarative memory
consolidation in children compared
with adults
Anna Peier1,2 ✉ , Maud Brichet1,2, Xavier De Tiège1, Philippe Peigneux2 & Charline Urbain1,2 ✉
Post-learning slow wave sleep (SWS) is known to support declarative memory consolidation. As SWS
is more abundant in young population, we suggested that sleep-dependent memory consolidation
processes could occur at a faster pace in school-aged children. After learning new associations between
non-objects and their functions, retrieval performance was tested in 30 children (7–12 years) and 34
adults (20–30 years) during an immediate (IR) and a delayed retrieval (DR) session separated by either
a Sleep or a Wake condition. Sleep led to stabilized memory retrieval performance only in children, not
in adults, whereas no age-related dierence was observed after a similar period of wakefulness. Hence,
our results suggest more ecient sleep-dependent declarative memory consolidation processes in
children compared with adults, an eect potentially ascribed to more abundant and deeper SWS during
childhood.
Children, particularly at school-age, have to learn and consolidate high quantities of new declarative informa-
tion (e.g. learning a vocabulary list in a foreign language) to respond adequately to environmental demands.
According to system consolidation theories, declarative knowledgeis progressively integrated into long-term
memory through brain plasticity processes generating functional and structural changes at the neural level1,2.
Both in adults3–8 and across development9, studies showed that sleep plays an active role in these plasticity-related
changes promoting memory consolidation processes. In particular, slow wave sleep (SWS) has been suggested
to trigger (i.e. elicit) the transfer of newly learned representations, initially stored in the hippocampal and
para-hippocampal areas, towards prefrontal brain areas for long term storage8,10–12. Childhood, compared with
adulthood, is not only characterized by a higher amount and variety of learning experiences supported by cere-
bral plasticity processes13,14 but also by a higher amount of SWS15–18. Compelling evidence suggests that children
(7–12 years old) spend signicantly longer proportion of their night sleep time in SWS (around 25 to 35%)
than adults (around 15 to 20%)15,18–21. As several studies suggested that SWS markedly contributes to declarative
memory consolidation processes across development and as SWS is more abundant in school-age children than
adults, it has been suggested that sleep-dependent memory consolidation processes may be more ecient and/or
accelerated in children than in adults22,23. In line with this proposal, it has been shown using magnetoencephalog-
raphy (MEG) that in 7–11 year old children, a 90-minute daytime nap is already sucient to trigger changes in
signal amplitude of the neural substrates related to the long-term storage of newly learned declarative material23.
Importantly, a similar brain reorganization associated with the course of memory consolidation was previously
observed in adults, but only days to months aer the initial learning session8,12.
At the behavioural level, the beneficial impact of sleep on declarative memory consolidation has been
observed in adults3,5,8,22,24, children22,25–27, and adolescents28 either through stabilized or improved memory reten-
tion performance at delayed recall (compared with immediate recall). Yet, to the best of our knowledge, only
three studies have compared the impact of sleep on memory consolidation performance between children and
adults22,29,30 and did not highlight a developmental advantage of sleep on memory consolidation performance.
For instance, Wilhelm et al. (2008)22 compared sleep-dependent declarative memory consolidation performance
1Laboratoire de Cartographie fonctionnelle du Cerveau (LCFC), UNI – ULB Neuroscience Institute, Université libre
de Bruxelles (ULB), Brussels, Belgium. 2Neuropsychology and Functional Imaging Research Group (UR2NF), Center
for Research in Cognition and Neurosciences (CRCN), UNI – ULB Neuroscience Institute, Université libre de Bruxelles
(ULB), Brussels, Belgium. ✉e-mail: anna.peier@ulb.ac.be; curbain@ulb.ac.be
OPEN
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between children aged 6–8 years and adults, using a classical word-pair associate learning task. Participants had
a better recall performance aer a night of sleep compared to a similar period of wakefulness. However, over-
night improvements in performance were similar between adults and children, despite a twice as large amount
of SWS in children than in adults during the post-training sleep period. Since pre-existing knowledge boosts
memory consolidation processes31–33, the authors explained this lack of eect by the imbalance of pre-existing
representations associated with the learning material between children and adults. Smaller amount of schemata
and knowledge associated to the newly learned material (i.e., word pairs) in children may have prevented observ-
ing a potential advantage of sleep on memory consolidation performance in the younger population compared
with adults22,34.
In this framework, the present study investigated the potential age-related advantage of sleep on declarative
memory consolidation performance using a learning task that allows a clear comparison between children and
adults, by minimizing the impact of pre-existing representations on the to-be-learned material. To do so, we
explored the impact of sleep on the consolidation of new associations between non-objects and their “magical”
function, a material that is equally novel for adults and children23,35. We hypothesize that aer controlling for the
impact of pre-existing representations, children (7–12 years) would exhibit larger gains in memory retention
performance (i.e., dierence between the number of correctly recalled items at the delayed vs. the immediate
retrieval sessions) than adults (20–30 years) over a night of sleep.
Results
Sleep and circadian parameters. Sleep parameters are reported in Table1.
Sleep duration did not dier between the Sleep and Wake groups (see Methods section) during the nights
preceding the experiment (Night-2, Sleep: 9.93 ± 1.25 vs. Wake: 10.03 ± 0.88 h; Night-1, Sleep: 10.12 ± 1.37 vs.
Wake: 10.38 ± 1.21 h), either in the children (all ps > 0.18) or in the adult (all ps > 0.25) g roups.
In children, the average sleep duration for the two nights preceding the experiment did not dier from their
average sleep time over the past month (N-2: mean ± SD 10.0 ± 1.1 h, p = 0.5; N-1: 10.2 ± 1.3 h, p = 0.015).
Although adults slept longer during N-2 than they did on average over the past six months, the average sleep
duration of N-1 did not dier from the average sleep time in the past six months (N-2: mean ± SD 8.9 ± 1.3 h,
p = 0.001; N-1: 8.3 ± 0.9 h; p = 0.17).
During the post-learning night (N-0), sleep duration did not dier from the average sleep duration in the
past six months, either for children (N-0: mean ± SD 9.3 ± 1.0 h, p = 0.62) or adults (N-0: mean ± SD 7.5 ± 0.8 h,
p = 0.11). However, on average children slept signicantly more than adults (p = 0.001).
Vigilance parameters. Vigilance parameters are reported in Table2.
Sleep Wake
Children Adults Children Adults
Duration <6
months (h) 9.43 ± 0.42 8.09 ± 0.92 9.7 ± 0.75 7.92 ± 1.03
Duration N-2 (h) 9.93 ± 1.25 9.03 ± 1.35 10.10 ± 0.99 8.79 ± 1.31
Duration N-1 (h) 10.12 ± 1.37 8.20 ± 1.08 10.37 ± 1.22 8.42 ± 0.69
Duration N-0 (h) 9.27 ± 1.00 7.53 ± 0.78 — —
Onset <6 months
(min) 20.00 ± 7.56 21.88 ± 19.65 19.33 ± 8.00 19.28 ± 12.58
Onset N-2 (min) 18.00 ± 17.09 21.38 ± 24.28 17.13 ± 12.32 24.28 ± 28.89
Onset N-1 (min) 22.00 ± 16.01 24.06 ± 28.89 14.67 ± 13.43 16.39 ± 13.92
Onset N-0 (min) 10.00 ± 9.45 32.81 ± 39.20 — —
Table 1. Sleep parameters. Mean (±SEM) amount of sleeping hours (duration) and the latency (minutes)
required to fall asleep (onset) for the last months, the two nights before the experiment (N-2 and N-1), and the
night between the experiment and the delayed retrieval session (N-0).
Sleep Wake
Children Adults Children Adults
Vigilance Index
(ms) −7.20 ± 40.67 −10.19 ± 16.70 2.88 ± 30.32 −5.34 ± 16.37
PVT session 1
(ms) 460 ± 87.66 341.25 ± 31.18 425.07 ± 66.72 352.94 ± 29.21
PVT session 2
(ms) 452 ± 85.48 331.06 ± 29.43 424.87 ± 55.02 347.61 ± 29.14
Table 2. Vigilance parameters. Psychomotor vigilance task (PVT). Mean (± SEM) for the vigilance index (ms)
obtained by subtracting mean reaction times (RTs) in the delayed session from mean RTs in the immediate
session (ms), PVT mean RTs at the rst session (1) and PVT mean RTs at the second session (2).
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A repeated measures ANOVA analysis was conducted on Reaction Times (RTs) with one within-subject factor
SESSION (immediate retrieval, IR vs. delayed retrieval, DR) and two between-subjects factors CONDITION
(Sleep vs. Wake) and AGE GROUP (Children vs. Adults). Results did not show any main eect of session or of
condition nor interaction eect between these factors (all ps > 0.10). A main eect of age group [F1,60 = 52.32;
p = 0.00001; η2 = 0,465] was observed, with faster RTs in adults than in children (Children: mean ± SD
440.8 ± 74.8 ms; Adults: 343.6 ± 30.2 ms). Hence, vigilance performance remained stable between both retrieval
sessions in both conditions for children and for adults.
Memory retention performance: age-related and sleep eects. A t-test for independent groups
showed that the number of trials needed to reach the successful criterion (60% of correct responses) in the
learning session did not dier between children and adults (Children: mean ± SD trials 1.57 ± 0.68 vs. Adults:
1.65 ± 0.54, p = 0.6, see Fig.1A). A Bayesian t-test for independent groups also supported the null hypothesis
(BF = 0.113), indicating that the learning task diculty was comparable between children and adults. Likewise, a
factorial ANOVA analysis conducted on IR performance with between-subjectsfactors AGE GROUP (Children
vs. Adults) and CONDITION (Sleep vs. Wake) did not show any main eect of AGE GROUP [F1,60 = 2.11;
p = 0.15; η2 = 0.034] or CONDITION [F1,60 = 3.18; p = 0.08; η2 = 0.050], nor an interaction eect [F1,60 = 2.61;
p = 0.11; η2 = 0.042], suggesting a comparable task diculty between age groups and conditions (see Fig.1B).
Descriptive analyses performed on retention indices (i.e., % correct responses at the DR – IR) showed that,
aer a night of sleep, children successfully recalled 1.87 ± 4.86% more denitions at DR in comparison with IR.
Aer the same night of sleep, adults forgot on average 4.75 ± 4.84% of the denitions they were able to retrieve
in the evening the day before (IR session). In the Wake condition, both age groups forgot a similar amount of
learned information between the DR and the IR sessions (Children: −2.53 ± 2.56%; Adults: − 4.67 ± 3.56%).
To statistically probe the eect of age on sleep-dependent memory consolidation, a factorial ANOVA analysis
conducted on the retention indices was performed with two between-subjects factors, namely AGE GROUP
Figure 1. Learning performance (mean ± s.e.m.). (A) Number of trials to achieve the success criterion of 60%
for children (N = 15) and adults (N = 16) in the Sleep condition and for children (N = 15) and adults (N = 18) in
the Wake condition. (B) Immediate retention performance (% of correctresponses for the immediate retrieval
session occurring directly aer the learning session) for children (N = 15) and adults (N = 16) in the Sleep
condition and for children (N = 15) and adults (N = 18) in the Wake condition.
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(Children vs. Adults) and CONDITION (Sleep vs. Wake). Results showed a main effect of AGE GROUP
[F1,60 = 18.45; p = 0.001; η2 = 0.235] and CONDITION [F1,60 = 4.49; p = 0.04; η2 = 0.070] as well as a signicant
AGE GROUP by CONDITION interaction [F1,60 = 4.85; p = 0.03; η2 = 0.075]. Post-Hoc Tukey tests showed that
in the Sleep condition, children had higher retention indices than adults (p = 0.00003), whereas retention indices
did not dier between age groups in the Wake condition (p = 0.06) (see Fig.2). e Bayesian t-test with AGE
GROUP as the between-subjects factor supported the hypothesis in the Sleep condition (BF = 4.36; p = 0.001)
and was not conclusive in the Wake condition (BF = 0.76).
Finally, correlation analyses showed that sleep duration and sleep onset on the experiment night were not cor-
related with the retention indices (Sleep duration: Pearson correlation (2-tailed) r = 0.164; p = 0.38; Sleep onset:
Pearson correlation (2-tailed) r = −0.05; p = 0.80) (Fig.2).
Discussion
is study demonstrates stronger overnight gains of declarative memory retrieval performance in children com-
pared with adults. Our results showed that aer a night of sleep, in children, memory retention performance
was stabilized (i.e., there was no memory loss, reecting successful consolidation22) between the immediate and
delayed retrieval sessions while memory retrieval performance decreased in adults. Importantly, delayed retrieval
performance decreased both in children and adults aer an equivalent interval of wakefulness, strengthening the
specic eect of sleep on the age-related dierences observed in our study.
Given the higher proportion of SWS in children than adults and considering the crucial role of this sleep
stage for memory consolidation9,15,18, several authors hypothesized a developmental advantage of sleep for mem-
ory consolidation processes in children22,23,34. Highly consistent with this hypothesis, our results are surprisingly
the rst to show this eect. Previous studies did not highlight improved sleep-dependent memory consolida-
tion performance in children compared with adults22,30. In these studies, the lack of age-related dierences on
sleep-dependent memory consolidation performance was explained bypotential unbalanced learning-related
pre-existing representations between children and adults22,34. Reinforcing this idea, animal studies showed that
larger schemas in long-term memory boost memory consolidation processes31,32.
is study addressed this issue by using a learning material that was equally novel for adults and children. is
allowed us to accurately compare age-related dierences of sleep on memory consolidation performance. Results
conrmed that both children and adults showed equivalent learning performance at the immediate retrieval
session and needed a similar number of trials to reach the successful learning criterion (60%). us, contrary to
previous studies, our results cannot be explained by an unbalanced task diculty between adults and children.
Sleep parameters and vigilance performance were also carefully controlled at each retrieval session in both age
groups. We observed comparable vigilance performance between retrieval sessions (IR vs. DR) and experimen-
tal conditions (Sleep vs. Wake) in children and adults. ese observations excluded a potential contribution of
circadian or vigilance eects on the observed sleep-dependent dierences between age groups. Sleep parameters
were also assessed by self-reported questionnaires and were equivalent between both age-groups apart from the
number of hours of sleep which was, as expected, higherin children thanin adults. Correlations between hours
of sleep and retention performance did not reach signicance, similarly to previous ndings suggesting that
retention performance may not be dependent on the total amount of sleep, but more specically on SWS rates36.
SWS has been related to hippocampal activation37 and hippocampus-dependent memory consolidation pro-
cesses6. Related to a dialogue between neocortical and (para)-hippocampal areas, it has been hypothesized that
SWS would trigger better memory consolidation by transferring new information from the hippocampus and
the para-hippocampus, the intermediate storage areas, to the neocortex for long-term storage and integration
into memory networks8,10,34. Remarkably, up to pubertal age, children show more SWS15,16 than adults. In this
respect, our results provide additional support for the crucial role of sleep for memory consolidation processes
during childhood. Our ndings suggest that age-related dierences in memory retrieval performance specically
observed aer a night of sleep are related to a benecial role of SWS for children compared with adults. Future
neurophysiological studies are needed to conrm this hypothesis.
Figure 2. Memory retention performance (mean ± s.e.m). Retention indices (percentage of correct responses at
delayed retrieval minus percentage of correct responses at immediate retrieval) in children (N = 15) and adults
(N = 16) in the Sleep condition and in children (N = 15) and adults (N = 18) in the Wake condition. Asterisks
indicate a signicant dierence between age groups (children VS adults): *p ≤ 0.05 or **p ≤ 0.01.
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We expected children to benet more from sleep than adults to consolidate memories, a prediction conrmed
by our data. However, an overnight decrease of performance in adults was unexpected, since several studies
showed a benet of sleep on declarative memory consolidation performance in adults8,22,26. One explanation
could be that, in adults, totally novel representations are poorly consolidated by post-training sleep, as prior
knowledge seems to be a prerequisite for new memories to be consolidated during sleep38–40. In that line, stud-
ies in rodents31,32 have highlighted a strong impact of retroactive interference on totally new representations.
New information related to pre-existing knowledge seems less sensitive to retroactive interference, and there-
fore features a slower deterioration rate. Moreover, the declarative memory network contribution to successful
memory retrieval is enhanced for the schema-congruent relative to schema-incongruent memories in adults39,40.
Interestingly, Brod et al. (2017) showed that hippocampal and neocortical contributions during a retrieval session
were not dependent on pre-existing knowledge in children. However, in adults, activation of the declarative mem-
ory networks signicantly depended on the congruence of the new information with prior learning41. Hence, in
line with these previous studies, our results suggest that pre-existing schemas wield a specic eect on memory
consolidation processes in adults, which does not seem to be the case in children.
In conclusion, the present study supports the importance of sleep and its impact on learning processes dur-
ing childhood. By comparing sleep-dependent memory consolidation performance between children and adults
diering on the amount of SWS15,16,18, and by showing the specic advantage of sleep in children on memory
consolidation performance, our experiment presumed to advance the study of brain mechanisms underlying
age-related changes in sleep-dependent memory consolidation processes. Hence, our ndings open up novel ave-
nues to investigate how age-related changes in SWS-dependent memory consolidation processes may be related
to dierent underlying neurophysiological processes in children and adults both in the context of typical or atyp-
ical developmental conditions.
Limitation section. We acknowledge limitations in the present study that could be addressed in the future.
First, we did not record electrophysiological sleep parameters and therefore could not quantify SWS in our young
and adult populations, or search for potential correlations with overnight changes in memory performance.
However, we believe that it does not hamper the validity of our main conclusions based on the known dierences
in SWS between prepubertal and adult populations. Over the past 15 years, developmental studies have consist-
ently demonstrated that the amount of SWS drastically decreases with age across the maturational process (see
Kurdziel, 20199, for a recent and detailed review on this topic). From 6 years old to prepubertal age, the SWS rate
as well as its dierent characteristics are quite similar despite age dierences17,18. Across puberty, SWS rate sharply
declines in association with a decrease of cortical connectivity resulting from brain maturation and reduced
synaptic density15,19,20 and continue to decrease with age16,18. For instance, Kurth et al. (2010) showed that while
prepubertal children (≤12 years old) exhibited a SWS rate of 28.1 (±2.8) % per night, mature adolescents already
showed a signicant decrease in SWS rate with 19.3 (±1.7) % per night21. us, according to these numerous
developmental studies and, as we compared school-age children (7–12 years) and adults (20–30 years), we assume
that SWS durations per night dier signicantly between populations without overlap in our study. We also chose
not to obtain EEG recordings in this study, to have children and adults sleeping in more natural conditions.
Second, due to the absence of interference in the sleep condition, one may hypothesize that sleep may act as a
“temporary shelter” that simply postpones the eect of interference and, thereby, passively maintains the mem-
ory traces. However, compelling evidence have critically challenged this view and showed that sleep-dependent
gains in memory performance do not solely result on the basis of reduced interference but depend on an active
role of sleep. At the behavioural level, Ellenbogen and coll. demonstrated in two important behavioural studies
not only that sleep improves recall of verbal memories despite the presence of retroactive interference but also
that sleep renders these newly formed memories more resistant, especially when it is challenged with interfer-
ence42,43. In addition to these studies, a great body of neurophysiological studies also demonstrate the active role
of sleep in consolidating memory. In particular, several studies showed, using polysomnographic recordings,
that sleep-dependent improvements in performance were associated with a specic sleep stage (e.g. SWS but not
REM sleep or Sleep stage 2)44–47. Furthermore, neuroimaging studies conducted in adults showed reactivation of
learning-related cerebral areas during sleep and that the amplitude of these activations were correlated with the
amount of overnight gains in performance6,48. Altogether, these studies demonstrated that sleep plays an active
role in declarative memory consolidation processes, thus, rejecting critics asserting that the benecial impact of
sleep on memory performance results from a passive and temporary protection against interference that would
otherwise be observed during wakefulness.
For future directions, we believe that further studies should investigate changes in sleep-dependent memory
consolidation processes across various developmental age groups, including younger children (<7 years old) and
adolescents (12–18 years old). is may also help better understand how sleep-dependent memory consolidation
changes may dierentially impact academic performance and general cognitive abilities. In particular, compar-
ing these aspects before and aer adolescence should provide us with important information, as a substantial
decrease in the SWS rate (for a similar night of sleep) occurs during this developmental period15,21,49–51. We also
suggest future work to investigate the link between sleep disorders and learning disabilities, as evidence shows
an association between atypical sleep patterns in children (e.g., interictal epileptic activity during slow sleep) and
memory diculties23,52–56.
Methods
Participants. e initial sample was composed of 87 participants including 39 adults (25 women; mean ±
SD age: 23,90 ± 2,12 years; range, 20–30 years) and 48 children (24 girls; mean ± SD age: 9,67 ± 1,78 years; range,
7–12 years). All participants and legally authorized representatives for participants age below 18 gave written
informed consent before their inclusion in this study approved by the local Biomedical Ethics Committee [CUB
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Hôpital Erasme - Université Libre de Bruxelles (ULB, 018/2016)]. All participants were native French speakers.
ey had no medication or neurological, learning or language disabilities or developmental delay history.
Participants were asked to respect their usual sleep habits at least the 2 nights preceding the experiment. Sleep
quality and sleep habits over the past month were assessed using the Pittsburgh Sleep Quality Index (PSQI)57 for
adults, or the Sleep Disturbances Scale for Children (SDSC)58 for children. To estimate the maintenance of the
sleep habits during at least two nights prior the experimental night and during the experiment, sleep duration
and latency were assessed using the St. Mary’s Hospital Sleep Questionnaire59. As retrieval sessions occurred at
dierent times of the day depending on the experimental condition, circadian chronotypes and vigilance states
were carefully controlled to avoid any time-of-the-day eect or vigilance variation on retention performance.
Circadian chronotype was assessed with the Morningness-Eveningness Questionnaire in adults (MEQ)60 and
with the Children Morningness-Eveningness Preference in children (CMEP)61. Participants with an extreme cir-
cadian chronotype were excluded.
Vigilance state was assessed at each retrieval (delayed and immediate) session using the Psychomotor
Vigilance Task (PVT, 5 minutes-duration version)62, according to standards in the eld63. Participants were asked
to press a button as fast as possible each time a digital counter started, with the reaction time as a depend-
ent measure. e PVT-task is a gold standard measure to detect changes in vigilance related to circadian varia-
tions62–64. e PVT is also routinely used in sleep and memory studies to control for a possible impact of variation
in vigilance state on learning and performance measures8,29,63–67. To control for such confound in our protocol, we
administered the PVT to our participants both in the morning and the evening sessions.
e nal sample was composed of 64 healthy subjects aer exclusion of participants with (i) abnormal sleep
habits, quantity or quality before or during the experimental night, (ii) extreme circadian chronotype, (iii) sig-
nicant dierence of vigilance between retrieval sessions. e nal sample included 34 adults (21 women; mean
± SD age: 23.8 ± 2,22 years; range, 20–30 years) and 30 children (17 girls; mean ± SD age: 9.7 ± 1,77 years;
range, 7–12 years). All participants were randomly assigned either to a sleep [Sleep, 15 children (mean ± SD age:
9.47 ± 1,64 years; 8 girls); 16 adults (mean ± SD age: 23.0 ± 2,39 years; 10 women)] or a wake [Wake, 15 children
(mean ± SD age: 9,87 ± 1,92 years; 10 girls); 18 adults (mean ± SD age: 24,5 ± 1,86 years; 11 women)] condition.
Adults received a nancial compensation while children received a gi voucher for their participation in the
study.
Materials. One hundred colored 2D outline drawings of unfamiliar non-objects (see Fig.3A) created by the
same artist and paired using PHOTOSHOP 2 in terms of size (6×6 cm on screen), intensity, colors and contrast
were used. Non-objects were directly adapted from two existing databases68. All the NO were presented on the
same 17 inch screen laptop for all participants, at a distance of 80 cm of the eyes, with a 4°x4° visual angle. e
idiosyncratic character of the to-be-learned material was conrmed by a pre-test performed with a separate group
of children (N = 37) to ensure that none of those non-objects were associated with any meaning. Each of the
non-objects was randomly associated with a denition of the object’s magical (imaginary) function (e.g., With
this object you can “open any doors”, “see through the walls”, “stop the rain”, “quickly heal wounds”, “read people’s
thoughts”). All denitions were in French and were 4 to 7 words long. Four lists of 50 to-be-learned stimuli (ran-
domly selected from the set of 100 non-objects) were created in counterbalanced order. One list was assigned to
each participant at the learning session (see Fig.3B). A complete description of the properties of the material and
learning task can be found in Urbain et al. (2013a, 2016).
Learning and Retrieval sessions and Experimental procedure. All participants were tested at home
during 3 sessions: a learning session, an Immediate Retrieval (IR) session and a Delayed Retrieval (DR) session.
All sessions were conducted in a quiet environment. In the Sleep condition, the learning and IR sessions occurred
in the evening while the DR session occurred in the morning aer a night of sleep. In the Wake condition, learn-
ing and IR took place in the morning, and DR in the evening without a sleep interval (see Fig.3C).
During the learning session, all participants learned the 50 “magical” functions of each non-object. e learn-
ing session included ten learning blocks during which each participant learned ve non-objects. For each learn-
ing trial, a non-object was presented on the computer screen by the experimenter who mentioned its magical
function aloud to the participant. en, each non-object was presented during 150 ms followed by 850 ms of a
white screen and nally a question mark indicating to the participant to repeat the function they had just been
taught (see Fig.3B). Aer each ve non-objects, a recapitulative test (including ve non-objects) was adminis-
tered. Feedback with correct responses was given to the participant during this ve-by-ve learning session but
not during the IR or DR session (see below; a detailed description of the learning procedure is provided in Urbain
et al., 2013a).
e IR session occurred immediately aer the learning session. During the IR session, the 50 non-objects were
again presented one by one randomly. As for the learning session, each non-object was presented during the IR
session for 150 ms, followed by 850 ms of a white screen, and then the question mark indicating to the participant
to formulate the answer (the most complete denition; or “I skip” in case of forgotten items). Participants had to
correctly retrieve at least 60% of the novel verbal associations during that IR session that followed the learning
session. If the participant did not achieve a 60% success rate, the learning session restarted only presenting the
forgotten items. Once the success criterion was reached, meaning that the participant succeeded in remembering
at least 30 denitions out of 50, the IR session was completed.
e DR session occurred at home, on average eleven hours (10–12 hours) aer the IR session and in exactly
the same conditions except that no success criterion had to be reached. To avoid potential eects of sleep inertia,
the DR session in the Sleep condition and the learning Session in the Wake condition occurred one hour aer
participants woke up.
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Data acquisition and analyses. Retrieval performance at IR and DR was encoded using a computer pro-
gram (MATLAB 6.1 R12.1, Mathworks, Sherbom, MA, 2004). Additionally, participants’ oral responses were
recorded for qualitative purpose. Statistical analyses were conducted using STATISTICA 12 soware (TIBCO
SOFTWARE, California, USA, 2016).
Declarative memory retention performance was computed using a retention index (%), subtracting the per-
centage of correct responses at DR from the percentage of correct responses at IR for each participant. Analyses
were then conducted using a factorial ANOVA on the retention indices with two between-subject factors AGE
GROUP (Children vs. Adults) and CONDITION (Sleep vs. Wake). Post hoc Tuckey tests were used to decompose
ANOVA eects. Bayesian t-tests analyses were also conducted to provide further evidence in favor of either the
null or the experimental hypothesis. Bayes Factors (BF) are interpretable as an odds ratio and a default mode
for Bayesian t-test69. A BF value less than 1/3 is viewed as strong supportive evidence for the null hypothesis
(i.e., no dierence between groups) whereas BF values > 3 strongly support the experimental hypothesis of
between-group dierences. An intermediate BF value (between 1/3 and 3) is viewed as inconclusive.
To ensure that memory performance at immediate and delayed retrieval sessions was not confounded by a
circadian eect in both conditions (Sleep: evening-morning vs. Wake: morning-evening) or vigilance state, vig-
ilance was assessed at each retrieval (delayed vs. immediate) session using the PVT task. Analyses consisted of
a repeated measure ANOVA on PVT mean reaction times (RTs) with a within-subjects factor SESSION (IR vs.
DR) and two between-subjects factors AGE GROUP (Children vs. Adults) and CONDITION (Sleep vs. Wake).
Student’s t-tests for independent samples (or if variance were unequal, Welch’s t-tests) were computed to assess
potential dierences between groups or conditions on sleep parameters or the number of trials needed to reach
the successful learning criterion. In the Sleep condition, correlational analyses were conducted between sleep
onset or sleep duration on the experiment night (N0) and memory retention indices.
e signicance level was set at p < 0.05.
Received: 10 December 2019; Accepted: 26 May 2020;
Published: xx xx xxxx
Figure 3. Experimental task and procedure. (A) Picture denition task: at each session, children and adults
were asked to provide the denition of the non-object presented on the screen. Responses had to be given
aer the appearance of the question mark (1 s aer stimulus onset). (B) Sample illustrations of the 50 non-
objects used. (C) Experimental protocol: children and adults had to learn the denition of the 50 non-objects
presented in the morning (Wake condition) or in the evening (Sleep condition) and directly retrieve it during
the immediate retrieval session. Psychomotor vigilance was also assessed using the 5-minutes of the PVT. Aer
a 10–12-h retention interval lled with sleep (children, N =15 ; adults, N = 16) or wakefulness (children, N = 15;
adults, N = 18), a delayed retrieval of the 50 magical functions associated to the non-objects occurred, followed
by the 5-minutes psychomotor vigilance task.
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Acknowledgements
is work was supported by a grant of the Fonds de la Recherche Scientique (FRS-FNRS, Belgium: CREDIT
DE RECHERCHE: n° 29149840) - project “e role of slow sleep oscillations and associated brain connectivity
mechanisms in memory consolidation and executive functions”.We would also like to thank Prof M. J. Taylor for
her precious help in proofreading the manuscript.
Author contributions
Conceived and designed the experiments: C.U. Performed the experiments: A.P. and M.B. Analyzed the data: A.P.
and C.U. Wrote the manuscript: A.P. and C.U. All authors reviewed the manuscript.
Competing interests
e authors declare no competing interests.
Additional information
Correspondence and requests for materials should be addressed to A.P. or C.U.
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