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Motor memory consolidation in children: The role of awareness and sleep on offline general and sequence-specific learning

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Abstract

Study aim : The purpose of this study was to investigate the role of sleep and awareness on consolidation of general and Sequence-Specific learning in children. Material and methods : Male participants (n = 48, 10 to 12 years old) were assigned to one of four groups based on awareness and sleep. Acquisition phase took place in the morning (wake groups, 8 ± am) or in the evening (sleep groups, 8 ± pm) followed by a 12 hours retention interval and a subsequent delayed retention test (1 week). Children in the explicit groups were informed about the presence of the sequence, while in the implicit groups were not informed about it. For data analysis in consolidation of general sequence learning and Sequence-Specific Consolidation phases, 2 × 2 × 2 and 2 × 2 × 3 ANOVA with repeated measures on block tests were used respectively. Results : The data provides evidence of offline enhancement of general motor learning after 12 hours which was dependent on sleep and awareness. Moreover, the information persistence after 1-week was significant only in sleep groups. The results also indicated that consolidation of sequence-specific learning was only observed after 12 hours in element duration and it was related to sleep and awareness. Conclusions : The results revealed that sleep wasn’t only an essential factor in enhancement of off-line sequence learning task after 12 hours in children, but performance of the children was dependent on awareness and sleep.
Biomedical Human Kinetics, 14, 83–94, 2022
DOI: 10.2478/bhk-2022-0011
Original Paper
Motor memory consolidation in children: The role of awareness
and sleep on ofine general and sequence-specic learning
Hamideh Iranmanesh1, Alireza Saberi Kakhki1*, Hamidreza Taheri1, Charles H. Shea2
1 Department of Motor Behavior, Faculty of Sport Sciences, Ferdowsi University of Mashhad, Mashhad, Iran; 2 Department
of Health and Kinesiology, Texas A&M University, College Station, TX 77843-4243, Texas, USA
Abstract
Study aim: The purpose of this study was to investigate the role of sleep and awareness on consolidation of general and Se-
quence-Specic learning in children.
Material and methods: Male participants (n = 48, 10 to 12 years old) were assigned to one of four groups based on awareness
and sleep. Acquisition phase took place in the morning (wake groups, 8 ± am) or in the evening (sleep groups, 8 ± pm) followed
by a 12 hours retention interval and a subsequent delayed retention test (1 week). Children in the explicit groups were informed
about the presence of the sequence, while in the implicit groups were not informed about it. For data analysis in consolidation
of general sequence learning and Sequence-Specic Consolidation phases, 2 × 2 × 2 and 2 × 2 × 3 ANOVA with repeated meas-
ures on block tests were used respectively.
Results: The data provides evidence of ofine enhancement of general motor learning after 12 hours which was dependent
on sleep and awareness. Moreover, the information persistence after 1-week was signicant only in sleep groups. The results
also indicated that consolidation of sequence-specic learning was only observed after 12 hours in element duration and it was
related to sleep and awareness.
Conclusions: The results revealed that sleep wasn’t only an essential factor in enhancement of off-line sequence learning task
after 12 hours in children, but performance of the children was dependent on awareness and sleep.
Keywords: Consolidation – Children – Ofine learning – Passage of time – Explicit knowledge
Introduction
Memory consolidation refers to the stabilization and
enhancement processes that can occur without any addi-
tional practice, intent, and/or awareness [24]. This process
can result in increased resistance to interference and an
improvement in performance following an ofine period
[26]. Therefore, memory consolidation involves two phas-
es: stabilization (behavioral performance maintenance)
and enhancement (also known as ofine learning). Ofine
learning commonly occurs after sleep without any training
or experience [2, 17, 35]. In fact, in this phase, a novel and
initially unstable task representation is strengthened and
stabilized in long term memory via sleep [9]. This nd-
ing is consistent with active system consolidation theory
and synaptic homeostasis hypothesis [4, 6, 36]. These
theories suggest that a passive process such as sleep can
provide optimal conditions for an effective and active
enhancement of memory and stable memory representa-
tion [1, 4, 6, 10].
Special attention has been given to the role of sleep
in learning and consolidation of motor skills, in particu-
lar, motor sequential skills [2, 5, 13,]. Motor sequential
skills are a type of procedural memory which are learned
through the repetition and practice of a sequential pattern
without the person’s attention to the learning. These skills
are a fundamental part in our learned motor repertoire,
ranging from simple to complex skills [29, 41].
Some studies demonstrated that performance of mo-
tor sequence tasks were improved when the ofine period
included being a sleep rather than awake, while encoding
and retrieval of memories took place preferentially dur-
ing waking [1, 2, 10, 18, 20, 41]. Many of these stud-
ies have concluded that sleep can promote integration of
newly acquired information into existing memory sche-
mas and as a result, it allows for better recall of informa-
tion [18].
Author’s address Alireza Saberi Kakhki, Department of Motor Behavior, Faculty of Sport Sciences, Ferdowsi University of
Mashhad, Mashhad, Iran askakhki@um.ac.ir
H. Iranmanesh et al.
84
As a matter of fact, sleep has an important role in con-
solidation of sequential motor skills from the childhood to
adulthood. Hence, many researchers have conrmed the
benet of the sleep in both declarative memory (verbalize
knowledge of facts and events, in which information re-
call is conscious) and procedural memory (skills memory)
in adults [2, 11, 15, 20, 27, 38]. Although motor learning is
an especially critical factor during childhood, sleep is es-
sential in children’s cognitive, behavioral, emotional, and
motor development and important links to memory and
cognition [16, 41]. However, remarkably little is known
about the inuence of sleep on motor memory processes
and learning especially in motor sequence learning during
childhood which is still unspecied [7, 35, 41].
Some researches expressed that both children and ado-
lescence’s performance improve in declarative memory
consolidation after one night sleep. However, this improve-
ment was not sleep related in procedural memory [7, 16,
31, 32, 41]. Other researchers found that sleep can be use-
ful both in children and adults’ declarative and procedural
memory consolidation after training for a new motor skill
[3, 41]. Some of these results contradict the observed nd-
ings in researches involving adult participants [7, 16, 32,
35, 41]. Some researchers such as Jongbloed-Pereboom
et al. [21] discovered that ofine learning was independ-
ent of age, while Fischer et al. [16] showed this factor was
connected to age.
Accordingly, sleep-dependent motor memory consoli-
dation in children is not well-specied. The underlying
reasons for such inconsistency in results are still unknown.
It seems that benets of sleep in enhancement of ofine
motor sequence learning depends on different factors. One
of these factors is the individual’s awareness of the task
regularities [2, 20, 33, 34, 37]. This may play an important
role in children’s motor learning and may also be an im-
portant factor in ofine enhancement. Learning new skills
with practice can be accomplished unintentionally, with
little to no awareness (implicit knowledge), or intention-
ally, with an individual’s conscious awareness of the regu-
larities of the task to be learned or rules and facts on how
to move (explicit knowledge) [2, 21, 33, 37, 42]. Lots of
evidence exists about the role of awareness in online and
ofine motor learning of adults [2, 11, 12, 33, 34, 38].
Some researchers believed that the process of the ex-
plicit knowledge in working memory and storing of de-
clarative knowledge in the rst stages of learning were es-
sential parts in the performance and learning of the motor
skills. On the other hand, some others expressed that lack
of explicit knowledge around the motor’s basics and regu-
larities did not have a negative impact on the learning proc-
ess, and even in physiological and psychological stress, it
could improve the performance. The results indicated the
benets of the implicit learning along with explicit learn-
ing in skills acquisition (online learning) [21, 37].
In ofine learning domains, Robertson et al. [33] were
the one of the rst to demonstrate that awareness of task
regularities impacts ofine motor learning. Subsequently
they presented awareness theory and also sleep-dependent
memory consolidation theory [33, 34]. They proposed that
when motor sequence learning was implicit, ofine en-
hancement only occurred in the passage of time. However,
in explicit conditions, improvement in performance only
occurred when the participants experienced sleep especial-
ly in the rst 12 hours after acquisition phase [2, 34, 38].
These theories have been conrmed with adult’s ndings
by a variety of tasks [2, 20, 21, 33, 38].
Sugawara et al. [35] suggested that sleep is associated
with ofine skill enhancement in explicit motor sequence
task in children, as in adults. Peiffer et al. [31] showed
overnight gains of declarative (explicit) memory reten-
tion performance in children. However, other researchers
showed that sleep, compared to wake in retention test, en-
hanced the consolidation of implicit motor sequence tasks.
These ndings were in contrast with the studies which
stated that sleep was only benecial in explicit skill learn-
ing [3, 11, 15].
It is noteworthy that relatively few studies have evalu-
ated implicit and explicit learning in children. Van Abs-
woude et al. [37] investigated the capacity of working
memory in implicit and explicit learning in children. They
found that after the ofine period, enhancement only oc-
curred in accuracy (not speed) in both implicit and explicit
learning conditions and minimal differences existed be-
tween explicit and implicit learning in children [37]. How-
ever, there is lack of evidence in children. Most studies in
this eld have been conducted on adults which manifested
the contradictory evidence on the role of sleep in implicit
sequence learning [2, 12, 20, 33]. Some researchers pro-
posed that implicit and explicit learning and their consoli-
dation in adults is different from children [37].
However, researchers, investigating procedural and
declarative memory in children, used simple tasks which
were naturally implicit (i.e., serial reaction time, implicit
continuous task) or explicit (i.e., two-dimensional objects
location, word-pair associates, nger tapping task) com-
pared to adults [3, 41]. However, implicit and explicit
knowledge of task instructions and regulations were typi-
cally not manipulated in these sequence tasks researches
[3, 7, 13, 16, 31, 41]. So, considering the little evidence in
children and not having enough investigations of the type
of knowledge relating to the task sequence, we cannot gen-
eralize the results of the adult researches to the children.
On the other hand, most of the studies investigating
consolidation in regard to children, evaluated the gener-
al improvement of the task related to sequence learning
[24]. General skill learning refers to increasing speed and
accuracy as a result of practice with the task, though re-
garding children, there exists another type of learning and
The role of awareness and sleep on ofine learning
85
consolidation following it, namely sequence specic
learning.
Sequence-specic learning refers to acquisition of
sequence-specic knowledge, which results in relatively
faster responses for events that can be predicted from the
sequence structure versus those that cannot (such as new
or random sequence) [24, 26, 37].
The vast majority of experiment on sequence learn-
ing have not reported any differences between the gen-
eral and sequence-specic learning especially in children.
Only a limited number of experiments have focused on
this issue. Research on young adults and older adults with
respect to implicit sequence learning conditions gener-
ally revealed that enhancement of general sequence learn-
ing had occurred. However, regarding sequence-specic
learning, no improvement was found in either age group
(young and elderly adults) or consolidation intervals (12,
24-hr & 1 week) [24, 25]. Also, the only research that was
done on children showed that improvement only occurred
in terms of accuracy (not speed) of general and sequence-
specic learning after one day [37]. However, in this eld,
there exists lack of evidence.
Moreover, most of the previous researchers investi-
gated the children’s consolidation process after acquisition
phase in a limited time [3, 7, 37, 41]. It is possible that
the little persistence of memories after sleep prevented the
benecial effects on the performance in a relatively short
period of time after acquisition phase, but after passage of
the additional time, performance enhancement might be
observed. Though, it is still not claried whether the over-
night gains are temporary or stable after passage of the
time in children.
Based on the above discussions, sleep dependent con-
solidation and its related effective factors like implicit and
explicit knowledge are rarely investigated. In fact, the role
of awareness in promoting motor sequence learning little
is known about whether explicit knowledge of sequence
enhances online and ofine motor sequence learning in
children. Some researchers believe that implicit learn-
ing is independent of age and cognitive resources. Con-
sequently, it has been recommend as superior to explicit
learning, especially for children [21, 37].
By investigating these factors, we can investigate the
theories and hypothesis related to the consolidation and
awareness of children in studying the effects of night sleep
immediately after the rst practice of motor sequential
skill. The separation of the enhancement of the general
skill from the enhancement of specic sequence in ofine
and online learning was not adequately addressed in the
literature.
Therefore, the purpose of the present research was
to evaluate the effect of children’s explicit and implicit
knowledge in a sleep-dependent consolidation of gener-
al and sequence specic motor sequence task. This task
involves dynamic arm movement task. It is important to
note that detecting xed sequence within this type of task
is more difcult than with a nger tapping and types of
serial reaction time tasks [8, 30]. Most of the tasks used
in children eld were simple and needed little motor re-
quirements (Press the key/button with ngers such as se-
rial reaction time task, nger tapping task, and button box
task). The task in the present study, due to the higher level
of processing requirements (containing more elements and
goals) and more motor needs (exion/extension move-
ments) were more complex than the previous motor se-
quence tasks [8, 29, 30]. Therefore, memorizing the infor-
mation and detecting sequence blocks were more difcult
for the participants [30].
Finally, the effects of the night sleep after skill acquisi-
tion in long term has little been investigated. Therefore,
this article has investigated not only the role of night sleep
immediately after the practice of motor sequence skill,
but it has also investigated the evaluation of the results of
night sleep with the passage of time after one week for de-
termining the resistance of dynamic arm movement task.
Material and methods
Participants
Right hand dominate children (N = 60, age, range:
10–12 years, mean: 10.84 ± 0.72) took part in the study.
Informed parental and child consents were obtained.
All children were asked to respond to a General Health
Questioner (Lndygraf and Abaz, 1996) and reported good
general health with no medical conditions, no history of
neurological and developmental disorders, no prior expe-
rience to the task, no recognized sleep problems and all
had normal IQ [3, 14]. They received a small gift for their
participation. The experiment was approved by ethics
committee of biological research of Ferdowsi University
of Mashhad (IR.MUM.FUM.REC.1397.11). Participants
were asked to respond to a hand dominance questionnaire
[28], Child Sleep Habit Questionnaire and Wechsler Intel-
ligence Scale for Children-Fourth Edition [14, 40]. Some
of the participants were omitted from the study: three of
which because of lack of sleep, four, of guessing the se-
quence in the implicit groups, three, of absence in the fol-
lowing 1 week test, one, of absence in retention of 12 hours
and one of them omitted because of fatigue and doing the
sequence falsely. Finally, 48 children were chosen.
Apparatus
The apparatus was Dynamic Arm Movement Task
(DAMT) which was adapted from Park and Shea task [30]
to evaluate motor sequence learning. DAMT consist of
horizontal lever and monitor (43 inches). The axle of lever
which rotated freely in ball-bearing supports, allowed the
H. Iranmanesh et al.
86
lever to move in the horizontal plane over the table sur-
face. At the distal end of the lever, a vertical handle was
attached. The position of the handle could be adjusted so
that when the participant rested their forearm on the lever,
with their elbow aligned over the axis of rotation and they
could comfortably grasp the handle (palm vertical). The
location of the participants’ hand on the lever was adjust-
able to their hands’ length [8, 29]. The horizontal move-
ment of the lever was monitored (1000 Hz) by increment
rotary encoder, which was attached to the end of the axle
of lever and stored for later analysis on computer. A point-
er was attached to the end of the lever extended, so that it
could be positioned within the targets on the monitor. Al-
so, to reduce the noise, nine optical sensors were used on
the main body of the apparatus under the lever to precisely
elaborate the movement. Another pointer was attached
vertically under the lever to make connection with optical
sensors. The distance between the pointer and the monitor
was 20 cm and the distance between the participants and
the monitor was approximately 80 cm [22, 30].
Procedures
Participants were randomly assigned to one of four ex-
perimental groups which differed in terms of the time of
day for acquisition testing (sleep and wake) and aware-
ness (implicit and explicit) of the sequence. The sleep
groups started acquisition phase at 8 PM (±1 hour) and
the wake groups started it at 8 AM (±1 hour) [41]. In the
explicit groups the participants were provided knowledge
about the order of the sequence elements and what trials/
blocks this sequence would be presented, but the implicit
groups were not informed of the repeating xed sequence
[33, 37]. The wake groups were not allowed to take a nap,
but the sleep groups were instructed to sleep after the ac-
quisition session [13, 24, 41].
The participants were seated on a chair facing the moni-
tor and the apparatus was adjusted, so that the participants’
lower arm was approximately on the 60-degree angle to
the upper arm at the starting position which arbitrarily
designated as 0-degrees. The range of the motion required
to complete the sequences was approximately 0 to 80 de-
grees from the start position. The participants had to move
the pointer to the targets displayed on monitor by exion
and extension of their arms [22]. The diameter of the tar-
gets represented 2 degrees of elbow extension/exion.
The targets (10 circles) were illuminated on the monitor
but only four of the targets (1, 4, 7, and 10) were actually
used in the sequence. To begin a trial, participants were
asked to move the lever to the start position. When the
home position was achieved, outlines of the targets were
illuminated and the rst target 20 degrees from start posi-
tion (Target 1) was illuminated. Targets 2–10 were spaced
at 6.67 degree increments. Before the acquisition phase,
participants completed one random block (R) in order to
get familiar with the task. Upon hitting the target (cross-
ing the boundaries of target circle) the illumination was
turned off and the next target was immediately illuminated
until the block was completed. If the participants missed
a target, the target remained illuminated until the partici-
pant returned the lever to the target position. After hitting
the last target in each block, a ‘’stop’ tone was presented
and the display of the targets was removed [22, 30]. Par-
ticipants were instructed to respond as quickly, smoothly,
and accurately as possible to the changing target location
that appeared on the screen by moving the lever from one
target to next [8, 22].
The acquisition phase included 10 training blocks with
96 targets in each block (12 elements × 8 repeat) with
a one minute rest between each block [24] .The order in
which the targets were illuminated in S12 – S4, and S6 – S8
and S10 was based on the predetermined pattern. In Blocks
R1, R5 and R9 the targets were illuminated in a random
order. The predetermined order of the goal sequence was
4,1,4,1,4,7,4,1,4,7,10,7 with the same distance between
each target (20 degrees). The same movement distances
were used in the random blocks but the target pattern was
changed [30]. To limit the participant’s ability to acquire
knowledge of the sequence the rst three elements of each
block were randomly presented and these elements were
omitted from the analysis [24].
Retention test were conducted approximately 12 hours
after the completion of the acquisition session. Fol-
low up test took place at the same time of day (Between
08:00–10:00 AM) after one week for all groups [13, 24].
Each test included three blocks (96 trials). The rst and
third blocks (S11 and S13 in the retention test and S14 and
S16 in the follow-up test) involved the same sequence as
used on repeated blocks in acquisition phase and the sec-
ond block (R12 in the retention test and R15 in the follow-
up test) included a random sequence [13]. The experimen-
tal design is shown in Appendix.1. Sleep duration and its
quality after acquisition phase were evaluated from par-
ents and children’s verbal reports [41].
Finally, at the end of the test, explicit knowledge of
sequence was examined by a brief interview with the par-
ticipants. They were asked if they had noticed anything
in particular about the stimulus locations and responses
[17]. They were asked to report the order of the repeated
sequence, either by guessing or from memory. The train-
ing sequence was judged to have been acquired if after the
experiment the participants correctly reported 6 or more
elements of the 12 elements training sequence [24]. In
addition, a recognition test was conducted with the par-
ticipants seated in front of the monitor and keyboard. Five
different demo sequences were shown with one of the se-
quences being the same as the one that they learned in the
1 Sequence Block.
The role of awareness and sleep on ofine learning
87
acquisition phase of the experiment. If they answered cor-
rectly, we concluded that they had acquired explicit and
declarative knowledge of the repeated sequence [30]. This
knowledge required conscious processing, and it was dif-
ferent from the processing method of implicit groups. This
was because the requirement for implicit learning was
non-conscious processing of the sequence orders such that
participant did not aware the pattern and order of sequenc-
es during the practice and recognition test [33, 34].
Data analysis
For data processing MATLAB software (Math works,
R2014a) was utilized and for statistical analysis SPSS 22
was used. Experimental variables included element dura-
tion and error of prediction. Element duration was com-
puted as elapsed time from hitting (crossing the target
boundary) of the currently illuminated target to hitting the
next illuminated target. Error of prediction was indicated
when a reversal movement was made away from the in-
tended target in a sequence. As a result, when an unneces-
sary reversal was observed in the movement displacement
while reaching to the goal, we concluded that the partici-
pants had misjudged the next target in the sequence.
Analysis of the data was performed for several differ-
ent phases that exist in this experiment with their corre-
sponding blocks. General improvement was determined
by analyzing changes in performance across the acquisi-
tion phase. Sequence-specic learning was determined
using the mean difference of element duration and error
of prediction between R9 and the average of S8 and S10
( R9-Mean (S8, S10)). Consolidation of general learning
was determined by comparing the last block of acquisi-
tion phase (S10) and the rst block of the 12-hour reten-
tion test (S11) and the comparison between the last block
of 12-hour retention (S13) and the rst block of the 1-week
retention test (S14). Consolidation of sequence-specic
was determined by comparing the sequence learning score
of acquisition phase (R9-Mean (S8, S10)) with sequence
learning score of 12-hour retention test (mean difference
between R12 and the average of S11 and S13 (R12-Mean
(S11, S13))) and sequence learning score of 1-week reten-
tion test (mean difference between R15 and the average of
S14 and S16 (R15-Mean (S14, S16))) [13, 24, 37].
The acquisition data (General improvement) was sub-
jected to a 2 (sleep, wake) × 2 (implicit, explicit) × block
(R1-S10) Analysis of Variance (ANOVA) with repeated
measures on block. Sequence-specic learning test was
analyzed with a 2 (sleep, wake) × 2 (implicit, explicit) ×
block (R9 and the average of S8 and S10) ANOVA with
repeated measures on block. The 12 hour retention test
(Consolidation of general learning) was analyzed with a 2
(sleep, wake) × 2 (implicit, explicit) × block 2 (S10, S11)
ANOVA with repeated measures on block and the 7 day
retention test was analyzed with a 2 (sleep, wake) × 2
(implicit, explicit) × block 2 (S13, S14) with repeated meas-
ures on block. Consolidation of sequence-specic learning
was analyzed with a 2 (sleep, wake) × 2 (implicit, explicit)
× block or sequence learning score (R9-Mean (S8, S10),
R12-Mean (S11, S13) and R15-Mean (S14, S16)) ANOVA
with repeated measures on block. Sidak post hoc test was
used to conduct multiple comparisons of means in within-
subjects effects in acquisition (General improvement of
task) and sequence-specic consolidation phases. Also, in
case of signicant differences between groups (between-
subjects effects) in consolidation of general sequence
learning phase, Scheffe post hoc test was used. The df2
were adjusted using the Greenhouse-Geisser correction in
case of violation of the sphericity assumption, i.e. when
the epsilon value was smaller than 1. Estimates of effect
sizes were analyzed using partial eta squared (η2
p). An al-
pha level of .05 was used for the analyses [24].
Results
Acquisition: General improvement of task
The analysis detected a main effect of block, for both
element duration, F5, 225 = 46.06, p < 0.01, η2
p = 0.51, and
error of prediction, F5, 225 = 7.06, p < 0.01, η2
p = 0.21. So
that, they were higher in R1, R5, and R9 than in the later
Blocks (S2–4, S6–8, and S10) where the repeated sequence
was presented. The results indicated an improvement in
speed and accuracy in repeated blocks (Figure and Table 1).
Moreover, the Block × Awareness in error of prediction
was also signicant (F6, 283 = 2.38, p < 0.05, η2
p = 0.05).
Figure and Table 1, show that explicit groups had lower
error of prediction than implicit groups. All other main ef-
fects and interactions failed signicance (p ≥ 0.05).
Sequence-Specic learning
The analysis detected a main effect of block (R9Mean
(S8, S10)), for both element duration, F1, 44 = 147.52,
p < 0.001, η2
p = 0.77, and error of prediction, F1, 44 = 5.78,
p < 0.05, η2
p = 0.12. So that, element duration and error of
prediction in the R9 (random sequence) were signicantly
higher than the average of S8 and S10. All other main ef-
fects and interactions were not Signicant (p ≥ 0.05, Fig-
ure 2).
Consolidation of general sequence learning
The results of the 2 × 2 × 2 ANOVA with repeated
measures on block indicated a signicant main effect of
block for both element duration, F1, 44 = 31.99, p < 0.01,
η2
p = 0.42, and error of prediction, F1, 44 = 5.87, p < 0.05,
η2
p = 0.12. So that, the element durations and errors of pre-
diction in S11 (beginning of session 2) were signicantly
2 Degrees of freedom.
H. Iranmanesh et al.
88
lower than S10 (the last block of acquisition). Moreover,
the Block × Sleep × Awareness in element durations were
also signicant (F1, 44 = 9.59, p < 0.01, η2
p = 0.17), in a way
that, decreasing trend of sleep-explicit group was signi-
cantly different from that of sleep-implicit and wake – ex-
plicit groups (Figure 1). All other main effects and interac-
tions failed signicance (p ≥ 0.05).
In addition, the results of the 2 × 2 × 2 ANOVA with
repeated measures on block in 1-week retention test
showed a signicant effect of block for element duration,
F1, 44 = 7.75, p < 0.01, η2
p = 0.15, indicating lower ele-
ment durations at the beginning of session 3 (S14) com-
pared to the end of session 2 (S13). The block × sleep was
also signicant, F1, 44 = 7.42, p < 0.01, η2
p = 0.14. So that,
trend of element durations in sleep and wake groups were
signicantly different (Figure 1). Hence, the 1-week con-
solidation of general sequence learning was sleep-depend-
ent. All main effects and interactions in error of prediction
failed signicance (p ≥ 0.05).
Sequence-Specic consolidation
The results of the 2 × 2 × 3 ANOVA with repeated
measures on block (sequence learning score) indicated
that the main effect of element duration was signicant,
F2, 88 = 11.52, p < 0.01, η2
p = 0.21. So that, the mean of se-
quence learning scores in session 2 (R12-Mean (S11 , S13))
and session 3 (R15-Mean (S14, S16)) were signicantly
higher than sequence learning scores in acquisition phase
(R9-Mean (S8, S10)). However, there was no main effect of
block in error of prediction, F2, 88 = 0.61, p ≥ 0.05. Hence,
S16R15S14S13R12S11S10R9S8S7S6R5S4S3S2R1
25
20
15
10
5
Block
Sleep-Explicit
Sleep-Implicit
Wake-Explicit
Wake-Implicit
S16R15S14S13R12S11S10R9S8S7S6R5S4S3S2R1
Element duration
Error of prediction
950
900
850
800
750
700
650
600
550
500
Block
Sleep-Explicit
Sleep-Implicit
Wake-Explicit
Wake-Implicit
Figure 1. The mean of element durations and errors of prediction (mean of 96 trails) in 16 blocks (R1 to S10 in acquisition
phase, S11 to S13 after 12 hours and S14 to S16 after the 1-week test) in four groups. (R: Random block, S: Sequence block)
(S8+S10)/2R9
22
20
18
16
14
12
10
8
6
Sleep-Explicit
Sleep-Implicit
Wake-Explicit
Wake-Implicit
(S8+S10)/2R9
900
850
800
750
700
Sleep-Explicit
Sleep-Implicit
Wake-Explicit
Wake-Implicit
Element duration
Error of prediction
Figure 2. The mean and standard error of element durations (in msec) and errors of prediction between block 9 (R9) and the
average of blocks 8 and 10 (S8, S10) in acquisition phase for Sequence-Specic learning
The role of awareness and sleep on ofine learning
89
these results showed ofine enhancement of sequence-
specic learning after 12 hours only accrued in element
duration.
The Block × Awareness in both element duration,
F2, 88 = 4.07, p < 0.05, η2
p = 0.08, and error of prediction,
F2, 88 = 3.79, p < 0.05, η2
p = 0.08, were signicant. So that,
the explicit groups recorded lower element durations of
sequence learning scores in acquisition session (R9-Mean
(S8, S10)) rather than the other conditions and they also
showed higher errors of prediction of sequence learning
scores in session 3 (R15-Mean (S14, S16)) rather than in
acquisition session (R9-Mean (S8, S10), Figure 3). Hence,
these results indicated that the ofine enhancement of
sequence-specic learning was dependent on awareness.
The block × sleep × awareness were also signicant in ele-
ment durations, F2, 88 = 3.41, p < 0.05, η2
p = 0.07. In ad-
dition, it was the only sleep-explicit group that recorded
higher element durations on sequence learning scores in
Block
Element duration Error of prediction
Sleep-
Explicit
Sleep-
Implicit
Wake-
Explicit
Wake-
Implicit
Sleep-
Explicit
Sleep-
Implicit
Wake-
Explicit
Wake-
Implicit
R1
Mean
SD
936.86
49.67
898.35
81.69
912.07
86.38
884.04
81.38
18.78
8.17
26.06
9.07
14.03
4.78
25.73
14.49
S2
Mean
SD
859.39
110.01
788.22
98.56
857.25
131.55
821.94
95.69
12.25
4.61
24.08
6.84
13.13
5.79
19.75
8.16
S3
Mean
SD
884.47
73.44
789.08
116.38
851.25
119.62
826.54
101.05
9.13
4.66
19.38
9.83
8.00
4.51
16.45
6.62
S4
Mean
SD
846.38
89.90
781.91
117.95
879.71
105.21
825.36
99.85
6.89
5.09
18.00
7.68
9.67
5.08
18.73
8.57
R5
Mean
SD
901.64
46.90
810.71
102.13
918.79
80.36
896.25
118.32
8.75
7.08
20.75
11.93
10.33
4.55
16.45
9.27
S6
Mean
SD
863.13
37.17
769.68
114.79
828.06
116.20
835.75
126.43
7.56
4.88
17.50
11.05
10.67
7.39
15.45
7.00
S7
Mean
SD
835.39
62.82
745.68
106.93
781.36
116.48
801.80
100.78
8.22
4.47
17.75
8.24
8.75
4.95
19.09
9.83
S8
Mean
SD
785.31
56.52
735.69
95.92
761.69
102.42
781.99
115.07
10.21
5.85
13.00
9.41
11.00
5.98
14.10
8.87
R9
Mean
SD
875.80
40.74
820.18
117.97
830.71
65.69
878.21
119.55
11.22
4.32
19.63
7.45
12.67
9.36
15.90
4.10
S10
Mean
SD
732.23
71.26
679.55
97.05
677.03
46.22
721.29
97.67
9.00
4.22
14.63
5.51
10.63
4.02
14.10
6.68
S11
Mean
SD
572.03
130.05
637.35
78.92
648.95
67.80
641.17
95.11
7.92
5.41
9.75
5.60
9.75
3.86
9.00
8.41
R12
Mean
SD
864.34
161.45
774.46
110.53
791.84
103.80
828.01
101.69
11.33
7.68
12.38
6.47
8.11
3.87
11.17
6.22
S13
Mean
SD
655.37
84.56
662.35
101.14
615.47
133.93
699.51
108.76
6.00
4.51
10.75
5.59
7.75
4.63
9.17
8.14
S14
Mean
SD
564.34
90.89
618.46
163.09
624.55
145.08
690.19
123.52
8.44
5.77
12.88
6.16
8.67
3.91
11.00
8.21
R15
Mean
SD
851.05
81.57
852.95
129.16
868.74
104.71
870.89
115.35
11.76
5.34
12.76
6.60
14.17
7.27
11.25
7.02
S16
Mean
SD
743.91
96.06
782.88
100.35
773.19
101.55
791.39
102.34
6.67
3.62
10.30
3.83
9.00
4.55
10.67
4.60
Table 1. The mean and standard deviation of element duration and error of prediction (mean of 96 trails) in 16 blocks (R1
to S10 in acquisition phase, S11 to S13 after 12 hours and S14 to S16 after the 1-week test) in four groups. (R: Random block,
S: Sequence block)
H. Iranmanesh et al.
90
session 3 (R15-Mean (S14, S16)) and session 2 (R12-Mean
(S11, S13)) rather than in acquisition session (R9-Mean
(S8, S10), Figure 3). All other main effects and interactions
were not Signicant (p ≥ 0.05).
Explicit knowledge
After completing the tests, four children from im-
plicit groups correctly reported elements of the repeated
sequence. Excluding these participants, the mean for
the repeated sequence was 2.87 elements correct out
of 12 which we take as chance level (expressing 4 ele-
ments or less than that was affected by the chance level)
(SD = 0.93, and n = 20). Also, these children answered
correctly in recognition test. As a result, they had explicit
knowledge of sequence rules and therefore were omitted
from the analysis.
Discussion
The purpose of this study was to investigate the role
of sleep and awareness on motor memory consolidation
with regard to general motor skill learning and sequence-
specic learning by assessments of performance improve-
ment between sessions in four groups (sleep-implicit,
sleep-explicit, wake-implicit, and wake-explicit).
Performance on session 1 (Acquisition phase)
In the rst session, children achieved general skill im-
provement in online learning by training the dynamic arm
movement task in all the groups. The response time and
error of prediction decreased in sequenced blocks. This
session indicates that repetition and adequate practice in
sequence skills increased speed and accuracy. These re-
sults implied that children’s performance improves with
more effort in training trails. So that, element duration and
error of prediction in the acquisition phase from the rst
to last sequence blocks decreased [8, 24]. Wilhelm [41]
showed that the average reaction times were decreased by
training.
However, except awareness in the error of prediction,
the type of knowledge and the training’s start time in the
acquisition phase (8 A.M. or 8 P.M) were not signicant
and general improvement occurred equally in all groups.
Although explicit groups recorded higher element dura-
tions than implicit groups in acquisition phase, these dif-
ferences were not signicant. The current research was ac-
cordant with studies that had not observed any differences
in response times between groups [5, 7, 21, 41]. This issue
suggests that children can improve general motor perform-
ance both with and without receiving explicit instructions
for the xed sequence [37].
The improvement trend for the motor sequence in er-
ror of prediction (contrary to the speed) among implicit
and explicit groups was different, such that the latter has
a lower error. Despite this, with practice, the decreasing
trend in the last sequence blocks was more than the rst se-
quence blocks in implicit groups. This happened when the
error in explicit groups during the practice had remained
constant and low. Some researchers showed that being in
the cognitive stage, could be the reason for the lower error
of prediction in the explicit groups. The main characteris-
tic of this stage was the conscious process of the informa-
tion related to the task. They believed that explicit groups’
awareness of the sequence pattern in error detection could
be the reason they perform better than implicit groups.
Due to implicit learning methods in implicit groups, they
were not involved in cognitive processes. Therefore, their
learning ability decreased in the performance error correc-
tion [21, 23].
R15-(S14+S16)/2R12-(S11+S13)/2R9-(S8+S10)/2
10
8
6
4
2
0
–2
Sleep-Explicit
Sleep-Implicit
Wake-Explicit
Wake-Implicit
R15-(S14+S16)/2R12-(S11+S13)/2R9-(S8+S10)/2
300
250
200
150
100
Sleep-Explicit
Sleep-Implicit
Wake-Explicit
Wake-Implicit
Element duration
Error of prediction
Figure 3. The comparison of mean and standard error of sequence learning scores (mean difference between Random block
and average of the adjacent sequenced blocks) in acquisition phase (R9-Mean (S8, S10)), after 12hr (R12-Mean (S11, S13)) and
after 1-week test ( R15-Mean (S14, S16))
The role of awareness and sleep on ofine learning
91
Also, the results in the sequence-specic learning
showed element duration and error of prediction in random
block (R9) were signicantly higher than the average of the
adjacent sequenced blocks (S8 & S10) in all of the groups.
When the speed and error increased in unpredictable tri-
als (random block) rather than predictable ones (repeated
sequence blocks), sequence-specic learning occurred in
children [24, 25]. In fact, when the random sequence was
presented, the response time was increased and more er-
rors occurred. This shows that children in implicit groups
had learnt at least some of the sequence. Therefore, Know-
ing the rules and regularities of a task does not necessarily
improve the performance and without that, the perform-
ance could be better than in random blocks [37].
Consolidation of general sequence learning
The results showed that children in all groups dis-
played slower response times and less errors of prediction
after 12 hours. Only the block × sleep × awareness in el-
ements duration were signicant. So that, the decreasing
trend of the elements duration in explicit-sleep group were
signicantly better than explicit-wake and implicit-sleep
groups, and there were not any signicant differences in
other groups. When the sequence is learnt explicitly
rather than implicitly or time-based, the consolidation is
sleep-dependent [2, 34]. The current results were consist-
ent with some research in children, adolescence and adults
which conrm that sleep had benecial role in the process
of declarative and cognitive procedural memory consoli-
dation [3, 33, 35, 38, 41]. Sugawara et al. [35] expressed
children’s sleep is related to the improvement of motor
sequence learning similar to adults. Wilhelm [41] and
Peiffer et al. [31] also conrmed that sleep was the main
factor of the declarative memory consolidation. Robertson
et al. [33], Ashworth et al [3], and van den Berg et al. [38]
mentioned that sleep would become the main role of the
performance improvement, if participants had learned and
practiced the regulation of the sequence task consciously.
Furthermore, when the children had practiced implic-
itly, the consolidation would be time-dependent. Some
researchers, contrary to the recent ndings, showed that
sleep after training session could enhance the perform-
ance of motor skills [3, 11]. Cho et al. [11] revealed that
adolescence’s accuracy, similar to adults, enhanced after
a night’s sleep. Ashworth et al. [3] also conrmed that
sleep would be benecial in enhancement of children’s
procedural memory consolidation.
These contradictory results were probably related to
the age, type, and nature of the task. Although, Ashworth
et al. [3] used the procedural memory task for evaluating
memory consolidation, only explicit aspects of the task
are consolidated by sleep, not the implicit ones. Along
this path, Janacsek and Nemeth [20] expressed that sleep-
dependent procedural memory consolidation was task-
related [20]. Moreover, participants of Cho et al. [11] re-
search were adolescence, whereas in the current research,
children were being studied. This is crucial, since age is an
important factor in the sleep dependent memory consoli-
dation of children [16].
These results were consistent with van den Berg et al.
[38] which expressed that sleep has an efcient role in the
cognitive process rather than a sequence task that is learnt
implicitly. Wilhelm [41] also realized that children, unlike
adults, showed less improvement in Finger Tapping Task
after one night sleep in retention test compared to awak-
ening. In addition, Fischer et al. [16] and Bothe et al. [7]
showed the same results. Al-Sharman and Siengsukon [2]
demonstrate that time, rather than sleep, appears to promote
off-line learning of an implicit continuous motor task.
This evidence conrmed the active system consolida-
tion theory [4, 6]. This theory expressed that during the
early phases of procedural learning, memory is considered
as an instable memory representation. Selected memory
contents are reactivated during sleep and transferred in-
to the long-term memory [4, 5]. Tononi and Cirelli [36]
in Synaptic homeostasis hypothesis expressed that al-
lowing the brain to go periodically “ofine” must serve
some important function. They suggested that during the
subsequent sleep, when external inputs are reduced, slow
oscillations renormalize these synapses inducing synaptic
depression. This leads to a weakening of unimportant and
less integrated information, making the important (signal)
relative to the spurious information (noise) more salient.
This process also restores the capacity of synapses to ac-
quire new information. Robertson et al. [33] and Song [34]
specied that ofine improvement after initial training
was affected by awareness. They mentioned that implicit
and explicit ofine learning are different and this differ-
ence was showed in the biological basis of acquisition
of skills during training. These two types of learning are
supported by two different mechanism: sleep-dependent
and time-dependent mechanism. In this regard, Janacsek
[19] expressed that cognitive functions were related to the
frontal lobe. Normal sleep is related to the cognitive func-
tion. This showed that sleep could be effective on cogni-
tive functions related to the frontal lobe and other areas of
the cerebral cortex. Meanwhile, implicit learning related
to the subcortical structure, had not benet from sleep.
Therefore, children in implicit groups activated subcor-
tical structures. It is logical that their consolidation was
time-dependent. Even though, the participants who learned
the sequence consciously followed by sleep, showed im-
provement in the retention test [2, 34].
Furthermore, the results showed that consolidation
of general sequence learning after 1-week occurred only
in elements duration. Some studies on adults conrmed
that consolidation of general learning was improved af-
ter 24-hours and one week [24, 25]. Desrochers et al. [13]
H. Iranmanesh et al.
92
demonstrated that motor sequence learning beneted from
sleep, but this was only evident after an extended period
of time in children under six years old. Also the result
showed that ofine enhancement of general learning after
1-week was sleep-dependent. Element duration in sleep
groups was decreased, but it was stable in wake groups.
This issue showed that immediate sleep after acquisition
of new skills would be an effective factor in persistence of
information in the passage of time [13].
Consolidation of sequence-specic learning
These results showed that ofine enhancement of se-
quence-specic learning was occurred only in the sleep-
explicit group after 12 hours in element duration. How-
ever, the sequence-specic consolidation didn’t occur in
error of prediction. In this way, Nemeth et al. [26] and
Meier and cock [24] showed that no improvement in se-
quence-specic learning was found in either age group,
training session or time interval in implicit tasks.
Walker et al. [39] realized that sequence-specic con-
solidation occurred by using Finger Tapping Task which
needed explicit knowledge of sequence. Van Abswoude et
al. [37] reported that improvement was occurred only in
accuracy (not reaction time) after 24 hours. Minimal dif-
ferences were found between implicit and explicit condi-
tion. These contradictory results might be related to the
age and task. Children in this study were under nine years
old and the capacity of their working memory didn’t ef-
fect in different types of learning. Children in the explicit
group gained more sequence knowledge than the implicit
group, and this knowledge did not transfer to a better se-
quence learning [37]. But in the current research, children
in explicit group which experienced sleep immediately
after training, gathered more information compared to im-
plicit and wake groups in dynamic arm movement task.
This matter caused a better transfer of sequence learning
in 12 hours after the training. As a result, even if sleep
didn’t have an essential role in sequence-specic enhance-
ment, it might be helpful in stabilization of memory traces
besides other factors such as awareness.
Conclusion
The results of the current study showed that sleep
wasn’t the only essential factor to enhance ofine motor
sequence task for children after 12 hours, and their per-
formance were related to both awareness and sleep. Of-
ine enhancement of general sequence skill learning was
sleep-dependent for explicit skills and time-dependent for
implicit skills. Although sleep immediately after acquiring
the new skills would be effective in information persist-
ency in the passage of time. Concerning this issue, for fu-
ture research, it is suggested to evaluate the other effective
factors on a sleep-dependent general and sequence-specif-
ic consolidation of children such as nature and different
types of tasks.
Conict of interest: Authors state no conict of interest.
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Received 25.07.2021
Accepted 06.01.2022
© University of Physical Education, Warsaw, Poland
Appendix 1. Experimental design of sequence learning in three phases: acquisition phase (Blocks: R1-S10), 12-retention test
(S11-S13) and 1-week retention or follow up test (S14-S16). Consolidation of general learning was determined by comparing S10
in acquisition phase and S11 in 12-hour retention test (1) and the comparison between S13 in 12-hour retention and S14 in 1-week
retention test (2). Consolidation of sequence-specic learning was determined by comparing the sequence learning score of
acquisition phase (mean difference between R9 and the average of S8 and S10) with sequence learning score of 12-hour retention
test (mean difference between R12 and the average of S11 and S13) and sequence learning score of 1-week retention test (mean
difference between R15 and the average of S14 and S16).
Note: R: Random block, S: Sequence block.
... Therefore, the goal of several studies in this area has been to identify crucial and efficient variables that encourage the acquisition of sequence knowledge to enhance its components more rapidly and precisely [5]. The kind of instruction is one of the most prevalent elements [17]. Originally, the majority of studies only employed explicit and implicit instructions, concentrating on strengthening the cognitive processes involved in comprehending the relative order of the elements of a sequence [15]. ...
... The criteria for entering the research include the age range of 18-21 years, being right-handed according to the Edinburgh Hand Dominance Questionnaire (Oldfield, 1971), having good general health status according to the Goldberg General Health Questionnaire (Goldberg, 1972), not having movement restrictions in the upper limbs based on the Box and Block Test (Mathews et al., 1985), not taking special drugs and not having physical and neurophysiological disorders and behavioral problems, not having previous experience in the desired task and having normal or modified natural eyesight. If the mentioned criteria were not met, the people did not fulfil the necessary criteria to participate in the research [3,17]. The participants entered the research procedure by signing the informed consent form after confirming their mental and cognitive health and fulfilling the requirements of the study. ...
... The apparatus was the Dynamic Arm Movement Task (DAMT), which was adapted from the Park and Shea task [17] to evaluate motor sequence learning. The apparatus consists of a horizontal lever and monitor (43 inches). ...
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