The role of nocturnal sleep on the retention, adaptability, and relearning rate of a motor skill

Abstract

Aim: The influence of sleep on the adaptability and relearning rate during learning of complex motor skills is still unknown, limiting the comprehension of the sleep role in motor memory consolidation. Thus, we aimed to investigate the nocturnal sleep influence on retention, adaptability, and relearning rate of the dart-throwing task. Methods: Sixty healthy adults were divided into two groups: SLEEP and WAKE. Both groups practiced an under-arm dart-throwing task. However, WAKE practiced in the morning and performed a retention phase in the evening, and SLEEP practiced in the evening and performed a retention phase in the morning of the next day. The practice and retention phases were separated by 12 h in both groups. There were analyses regarding retention (retention test), adaptability (delayed transfer test), and relearning rate (savings). Results: Both groups improved their performance across the acquisition phase and maintained it in the retention test. The groups did not demonstrate adaptability and did not demonstrate a significant difference in relearning rate. Conclusion: We conclude that nocturnal sleep did not modulate the consolidation of motor memories related to ballistic discrete motor skills.

Full text

Neural Control of Movement
The role of nocturnal sleep on the retention, adaptability, and relearning
rate of a motor skill
Fernanda Yngrid Martins Sousa
1
, Yasmin de Melo Rocha e Silva
1
,
Ana Kariele da Silva Santos
1
, Gisele Carla dos Santos Palma
2
,
Renata Louise Ferreira Lemos
1
, Giordano Marcio Gatinho Bonuzzi
1,3
1
Universidade Estadual do Piauí, Departamento de Educação Física, Picos, PI, Brazil
2
Universidade de São Paulo, Escola de Educação Física e Esporte, São Paulo, SP, Brazil
3
Universidade Federal do Vale do São Francisco, Programa de Pós-Graduação em Educação
Física, Petrolina, PE, Brazil.
Associate Editor: Angelina Zanesco .
1
Universidade Metropolitana de Santos, Faculdade de
Medicina, Santos, SP, Brazil;
2
Universidade Estadual Paulista “Júlio de Mesquita Filho”,
Departamento de Educação Física, Instituto de Biociências, Rio Claro, SP, Brazil. E-mail:
angelina.zanesco@unesp.br.
Abstract - Aim: The inuence of sleep on the adaptability and relearning rate during learning of complex motor skills
is still unknown, limiting the comprehension of the sleep role in motor memory consolidation. Thus, we aimed to
investigate the nocturnal sleep inuence on retention, adaptability, and relearning rate of the dart-throwing task. Me-
thods: Sixty healthy adults were divided into two groups: SLEEP and WAKE. Both groups practiced an under-arm
dart-throwing task. However, WAKE practiced in the morning and performed a retention phase in the evening, and
SLEEP practiced in the evening and performed a retention phase in the morning of the next day. The practice and reten-
tion phases were separated by 12 h in both groups. There were analyses regarding retention (retention test), adaptability
(delayed transfer test), and relearning rate (savings). Results: Both groups improved their performance across the
acquisition phase and maintained it in the retention test. The groups did not demonstrate adaptability and did not
demonstrate a signicant difference in relearning rate. Conclusion: We conclude that nocturnal sleep did not modulate
the consolidation of motor memories related to ballistic discrete motor skills.
Keywords: sleep, consolidation, motor memory, discrete motor skill, motor learning.
Introduction
Motor learning is a set of processes associated with prac-
tice or experience leading to relatively permanent changes
in the capability for skilled movement
1
. During motor skill
acquisition, practice-dependent behavioral improvements
are derived from changes in functional networks in the
Central Nervous System (CNS), which are recognized as
motor memories
2,3
.
Motor memory creation is a time-dependent process,
mainly composed of three phases: encoding, consolida-
tion, and retrieval
3,4
. Encoding is the initial phase when
the memory engram creation occurs
5
; for motor memories,
the encoding mainly happens during practice
3
. Consolida-
tion is the post-practice phase when the memory becomes
more robust and stable with less susceptibility to inter-
ference
4,6
. Then, savings of the improvement achieved
during practice (retrieval) is consolidation-dependent
2,7,8
.
Therefore, the relative permanence of the improved per-
formance which characterizes motor learning is mainly
developed during the consolidation phase
3,8
.
It has been suggested that motor memory consolida-
tion occurs during wakefulness periods that are temporally
close to practice and during sleep
8,9
. In this way, it is sup-
posed that sleep has a critical role in motor memory con-
solidation and consequently in motor learning
10-13
.
Several behavior-based studies identied that noc-
turnal sleep stabilizes
14
or even enhances
15-17
motor per-
formance after practice. Interestingly, some ndings
demonstrated that whole-body and complex motor skills
are more susceptible to consolidation sleep-dependent
mechanisms
14,18
than less complex motor skills, such as
nger sequences
19
or continuous motor tracking tasks
20
.
In fact, there is a call to action in the Motor learning area
to use complex motor skills as the to-be-learn motor task
in the experiments. Given that, the principles created by
simple task studies are not generalized to complex motor
skills
21
, such as sports skills and activities of daily living.
DOI: http://dx.doi.org/10.1590/S1980-657420220017221 Motriz, Rio Claro, v. 28, 2022, e10220017221

Only one study with complex motor skills (dance
routine implanted on a video game - PlayStation 2, Game
Dance Stage) veried whether the nocturnal sleep inu-
ences the adaptability of the improved performance to a
new variety of performance contexts characteristics
22
. In
this case, the nocturnal sleep did not impact the perfor-
mance of a new sequence of a dance routine. However, in
this study, Genzel et al.
28
did not verify the effect of sleep
on the adaptability of the motor task practiced; instead,
they investigated whether sleep inuences the transfer to a
new motor skill (a new dance routine). Therefore, the
effects of sleep on the adaptability of a motor task pre-
viously practiced still is unknown.
Also, an interesting aspect that is still unlled in this
literature is whether sleep can impact a subsequent prac-
tice. It has been postulated that reacquiring a skill that has
already been learned once before (but then apparently for-
gotten or partly remained) is typically faster than learning
it the rst time, being this phenomenon called savings
2
.
Also, to the best of our knowledge, no studies have
directly tested the inuence of nocturnal sleep on savings.
Regarding Christina
23
, there is an improvement in the
inference about motor memory construct underlying lear-
ning and retention as more than less performance informa-
tion is known
23
. Therefore, including savings and transfer
measures can benet motor learning inferences (for a
review about transfer, savings, and retention in motor
learning inference, see Christina and colleagues
23-25
).
In this way, we aimed to investigate the inuence of
nocturnal sleep on complex motor skill learning. More
specically, we assess the impact of the nocturnal sleep on
1- retention, 2 - adaptability through a transfer test, and 3 -
relearning (savings). Based on previous studies, we hypo-
thesized that a nocturnal sleep would enhance the persis-
tence and adaptability of the improved performance, and it
would induce a faster relearning rate.
Methods
The ethics board from the State University of Piaui
approved this study (protocol number.
30227720.0.0000.5209). All participants signed the con-
sent term before participation. There were no monetary or
other types of compensation to participate in this study.
All experiment was conducted following Helsinki
Declaration.
Participants
We recruited 60 participants from the local uni-
versity community, aged 18-39 years old (M = 25.35;
SD = 5.65), 31 men and 29 women. The inclusion criteria
were: 1 - Visual, neuromotor, and cognitive conditions for
understanding and executing the proposed tasks; 2 - Right-
handed regarding the Edinburgh Handedness Inventory
26
.
The exclusion criteria were: 1 - Osteoarticular diseases or
disfunction which unviable the performance of the pro-
posed activities; 2- Do not use a corrective lens in case the
participant has unsatisfactory visual acuity; 3 - Previous
experience in the dart-throwing task. 4 - The participants
were oriented to have good nocturnal sleep one day before
and during the experiment. They needed to have 7-9 h of
nocturnal sleep and subjectively perceive the nights of
sleep as satisfactory to recover for the next day. There was
no participant removed concerning this last criterion.
Instruments and tasks
The participants practiced an underarm dart-throw-
ing task used in previous motor learning studies (i.e., Al-
Abood et al.
27
). The task goal was to score as many points
as possible by throwing darts (Winmax® WMG50374)
with the dominant arm towards a target dartboard. The tar-
get was placed on the oor 3 m away from a throwing line.
The darts had 30 g and a length of 15 cm. The target con-
tained ten concentric circles, with the middle circle having
a diameter of 2.25 cm, with each other circle increasing by
2.25 cm in radius. We determined 10 points to trials that
hit the bullseye with each concentric circle radiating out
from the decreasing by one point. Hence, the outermost
circle was awarded only one point. If the dart hit the out-
side of the target, it was attributed 0 points.
Design and procedures
After the participants signed the informed consent,
they were randomly allocated into two groups: the Sleep
Group (SLEEP) (n = 30), which had a nocturnal sleep
between the acquisition phase and the retention phase, and
the Wakefulness group (WAKE) (n = 30) that completed
the acquisition phase and retention test in the same day.
To characterize the chronic sleep condition of the
participants, rstly, they answered the Pittsburgh Sleep
Quality Index (PSQI). After, they received instructions
about the motor task. Regarding the task's goal, the parti-
cipants received the following verbal instruction: “try to
throw the dart as accurately as possible into the center of
the target”. Also, they received visual instruction concern-
ing the movement parameters through a video of a skilled
person performing the task.
After the instructions, the participants performed 3
trials to familiarize themselves with the task. Following,
they completed a pre-test composed of 5 trials. The acqui-
sition phase was composed of 115 trials organized in 23
blocks. The participants rested 1 minute among the blocks
of practice to avoid deleterious effects from fatigue. After
practice, the participants performed a post-test with simi-
lar conditions to the pre-test. After 12 h from the post-test
began the retention phase, the participants performed a
retention test identical to the pre-test and post-test. Then,
the participants performed a delayed transfer test at a dis-
tance of 4 m to the target, composed of 1 block of 5 trials.
Finally, the target was reallocated to 3 m away from the
2 Sleep and motor learning

participants; then, the participants performed 24 blocks of
5 trials interspersed with 1 minute of rest to assess the
relearning rate (savings).
The unique aspect that differentiated the SLEEP and
WAKE was the time of day that the acquisition phase and
the retention test were allocated. The WAKE performed
the acquisition phase between 7:00 and 8:00 am, and the
retention test was performed at night on the same day,
between 7:00 and 8:00 pm. SLEEP had the acquisition
phase between 8:00 and 9:00 pm, and the retention test
was performed between 8:00 and 9:00 am on the follow-
ing day. The participants were oriented to wake up 1 h be-
fore the tests in the morning. The general experimental
design can be checked in Figure 1.
Measures
We assessed the motor performance of the partici-
pants through Root Mean Square Error (RMSE), being the
total amount of “spread” of the movements about the tar-
get, so it represents an overall measure of how successful
the performer was in achieving the target
1
, through the
equation:
RMSE =ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
Xxi−Tð Þ2=n
q
where x
i
= score on trial i, T = score maximum of the tar-
get, n = number of trials.
Statistical analysis
We used STATISTICA 11.0 (StatSoft Inc., Tulsa,
OK, USA) and Microsoft Excel 365 software for statistical
analyses adopting a 5% signicance level. We evaluated
the normality and homogeneity of the data with the Sha-
piro Wilks and Levene tests, respectively. We compared
TSQI (sum of the components) between the groups using
the Student's t-test.
We performed an ANOVA two-way - 2 groups
(SLEEP, WAKE) x 4 times (pre-test, post-test, retention
test, and transfer test) with RMSE to verify whether sleep
inuenced motor improvement, retention, and adapt-
ability. Tukey test was used for post hoc analyses. We
evaluated the savings by computing the number of blocks
of trials required for the participants to reach the mean
performance achieved in the post-test during the savings
phase. Next, we compared the number of blocks between
SLEEP and WAKE through a Student's t-test.
Lastly, we addressed whether the chronic quality
sleep identied by TSQI inuences the consolidation pro-
cess of the SLEEP, comparing the RMSE in the retention
test between individuals with poor and good sleep quality
through a Student's t-test.
Result
Regarding the PSQI, there was no signicant diffe-
rence between SLEEP and WAKE for the sum of the com-
ponents (p = 0.12; SLEEP M = 4.76, SD = 2.56; WAKE
M = 5.96, SD = 3.40). In the SLEEP, 11 participants had
poor sleep quality, while 19 had good sleep quality; for
WAKE, 14 participants had poor sleep quality, and 16 par-
ticipants had regular sleep quality.
Analyzing the RMSE in comparing the pre-test,
post-test, retention test, and transfer test (Figure 2), the
two-way ANOVA did not demonstrate interaction effects
and statistical signicance in the Group factor. However,
the Time factor was statistically signicant (F
1,58
= 4.79,
p < 0.01, η
2
= 0.07). The Tukey post hoc test revealed
that the post-test (p = 0.01) and the retention test
(p < 0.05) differed signicantly from the pre-test. There
Figure 1 - Experimental design timeline.
Sousa et al. 3

was no signicant difference between the pre-test and
transfer test (p = 0.91), indicating that groups did not
demonstrate adaptability independently of the nocturnal
sleep occurrence. Thus, our ndings indicated that
SLEEP and WAKE improved their performance, main-
tained it in the 12 h-retention test, and did not demons-
trate adaptability in the delayed transfer test, without
difference between them.
Lastly, our savings analysis through the students’ t-
test revealed no signicant difference between SLEEP and
WAKE regarding the relearning rate (p = 0.88, SLEEP:
M = 3.56, SD = 4.76, WAKE: M = 3.40, SD = 3.71)
(Figure 3). These ndings indicate that nocturnal sleep did
not impact the relearning rate (savings) of a motor skill
previously practiced.
Finally, there was no signicant difference for
RMSE in the retention test between SLEEP participants
classied with good and poor sleep quality in PSQI
(p = 0.12; poor: M = 7.85, SD = 1.23, good: M = 8.04,
SD = 1.08), which suggests that the chronic quality sleep
did not inuence the consolidation process of the SLEEP.
Discussion
We investigated whether nocturnal sleep inuences
the learning of a complex discrete motor skill. We adopted
an experimental design that allowed us to infer the noctur-
nal sleep role in the retention, adaptability, and relearning
rate. Our ndings revealed that nocturnal sleep did not
inuence the retention, adaptability, and relearning rate.
The SLEEP and WAKE groups demonstrated motor learn-
ing with the same behavior, which did not corroborate
previous studies.
Given that motor learning is a process composed of
improvement (gains in motor performance derived from
practice), consistency (performance becomes increasingly
more consistent), persistence (relatively permanent impro-
vement in performance), and adaptability (the improved
performance is adaptable to a variety of performance con-
text characteristics)
28
. Our study was the rst that includes
a complete inference about the essential characteristics of
the performance across the motor learning processes in the
experimental design. Previous studies did not include
transfer tests and savings analyses in their experiments,
which may induce an incomplete assessment of motor
memory creation
25,29
.
Even with the lack of inference about adaptability
and savings in previous studies, the inuence of sleep on
motor memory consolidation and motor learning is con-
sistently conrmed
10,12,13
. The difference between our
ndings with the previous studies can be related to the fact
that the inuence of sleep on motor memory consolidation
is task characteristic-dependent
10
.
It has been supposed that tasks with a strong cogni-
tive component tend to be supported by sleep-dependent
processing
30
, which may explain why complex and whole-
body motor tasks are more inuenced by sleep-dependent
ofine processes, given their higher cognitive demand
12
. It
has been suggested that some neuronal circuits involved in
motor learning are consolidated in the wakefulness period
while others are sleep-dependents
4,5,8
.
One aspect that maybe be related to the difference
between our ndings and the previous results in the litera-
ture is the task characteristics. In our study, we assessed
the role of nocturnal sleep in the learning of a discrete
motor task. In contrast, previous studies used bimanual
arm movements
31
, shooter video game task
32
, bimanual
nger tapping tasks
15
, unrestricted reaching task with the
Figure 2 - Performance on the underarm dart-throwing task as assessed
by root means square (RMSE) across practice, retention, and transfer
period. Data are presented as mean and 95% condence interval by each
group. * = signicant difference in Time factor in comparison to pre-test.
Figure 3 - Number of blocks during the relearning phase needed to
achieve the post-test mean performance for each participant. Data show
the mean (solid line) and individual data (dots).
4 Sleep and motor learning

non-dominant hand involving horizontal displace-
ment
16,33
, dance choreography in a videogame appara-
tus
22
, nger tapping task, pursuit tracking task, and
countermovement jump (60% of individual maximum)
14
,
and a locomotor task under dual-task requirement
17
. Ana-
lyzing all these studies, just one did not report the diffe-
rence between wakefulness and nocturnal sleep in the
retention test
14
. This study used a countermovement jump
task (60% of individual maximum), a discrete task as the
underarm dart-throwing task. Nocturnal sleep improved
motor consolidation for all motor tasks (serial or conti-
nuous), inducing a better retention test.
Classical studies already had signalized that discrete
motor skills demonstrate less retention than continuous
motor skills
34,35
. Two hypotheses have been used to ex-
plain this phenomenon
1
: 1 - Discrete motor skills have
more cognitive demands that are less robust to the for-
gotten than motor components, 2 - The practice of discrete
motor skills typically consists of a single adjustment or
action, receiving less amount of motor practice than conti-
nuous tasks, for example.
However, a third hypothesis can be created based on
our and previous ndings. We suppose that the consolida-
tion of discrete motor skills is less susceptible to sleep-
dependent processes, allowing less robustness against for-
getfulness for this type of motor memory. In this way,
neurocognitive ndings have indicated parallel neural net-
works to process and store movement components and
goal components of the motor skill to be learned
6,36,37
.
Additionally, the goal component is processed and stored
during sleep, while the movement component is wakeful-
ness-dependent
4,6
.
The primary mechanism to improve the motor per-
formance of discrete motor skills (such as countermove-
ment jump and dart-throwing tasks) is to enhance the
movement component (parameterization of force and
speed) because the goal component remains the same
among the trials (jump in a specic height or throw it into
the center of the target). This task-specic demand could
induce a lower effect from the sleep-dependent consolida-
tion processes for discrete motor skills, which explains our
results compared to previous studies.
Further investigations can address the effect of the
nocturnal sleep on the consolidation of different complex
motor tasks (serial, discrete and continuous tasks) to verify
whether the characteristics of the task inuence the sleep-
dependent consolidation participation. These further stu-
dies should include transfer tests and saving analyses to
verify the motor memory creation process, as we did in
this study.
In our study, we controlled the amount of sleep in the
SLEEP group (7-9 h), the chronic quality of the sleep
through the Pittsburgh Sleep Quality Index (PSQI), and
the time to wake up before the retention test (1 h). Ho-
wever, we did not control the sleep quality between the
acquisition phase and retention test for SLEEP. It can be
interpreted as a limitation because sleep quality inuences
the potential of motor memory consolidation
17,38
.
We adopted a “varied time design” (AM-PM versus
PM-AM) to study the role of sleep on motor memory con-
solidation. It has been well documented that the circadian
cycle is a covariable in this design
39
. However, other
designs also have their limitations. For example, using nap
as an independent variable with two groups practicing at
the same period can avoid the inuence of the circadian
cycle
39
. However, nap design does not engage the same
nocturnal sleep mechanisms
10
. Also, we have the “depri-
vation design”
39,40
, which both groups practiced in the
evening and tested on the following day. Though, one
group remains without sleep. In this case, we could control
the circadian cycle effects, but we have the detrimental
somnolence effect on the retention test for the experi-
mental group
10,39
. Further studies may include different
experimental designs (varied time, nap, and deprivation)
to provide a complementary comprehension of the sleep
role in learning complex motor skills.
Conclusion
Our results suggest that nocturnal sleep does not
inuence the learning of a discrete motor skill. Speci-
cally, nocturnal sleep does not affect the retention, adapt-
ability, and relearning rate of a discrete motor skill. We
believe that the consolidation process of discrete motor
skills is mainly based on wakefulness-dependent con-
solidation processes, given the low demand for movement
components of discrete motor skills compared to serial or
continuous motor tasks.
References
1. Schmidt RA, Lee TD, Winstein CJ, Wulf G, Zelaznik HN.
Motor control and learning: a behavioral emphasis. 6th ed.
Champaign, Human Kinetics; 2019.
2. Krakauer JW, Hadjiosif AM, Xu J, Wong AL, Haith AM.
Motor learning. Compr Physiol. 2019;9:613-63. doi
3. Kantak SS, Winstein CJ. Learning-performance distinction
and memory processes for motor skills: a focused review
and perspective. Behav Brain Res. 2012;228(1):219-31. doi
4. Robertson EM. From creation to consolidation: a novel fra-
mework for memory processing. PLoS Biol. 2009;7(1):
e1000019. doi
5. Robertson EM, Cohen DA. Understanding consolidation
through the architecture of memories. Neurosci. 2006;12
(3):261-71. doi
6. Cohen DA, Pascual-Leone A, Press DZ, Robertson EM.
Off-line learning of motor skill memory: a double dissocia-
tion of goal and movement. Proc Natl Acad Sci. 2005;102
(50):18237-41. doi
7. Krakauer JW. The applicability of motor learning to neuro-
rehabilitation. In: Oxford textbook of neurorehabilitation.
New York, Oxford University Press; 2015. p. 55-64. doi
Sousa et al. 5

8. Krakauer JW, Shadmehr R. Consolidation of motor mem-
ory. Trends Neurosci. 2006;29(1):58-64. doi
9. Foster DJ, Wilson MA. Reverse replay of behavioural
sequences in hippocampal place cells during the awake
state. Nature. 2006;440(7084):680-83. doi
10. King BR, Hoedlmoser K, Hirschauer F, Dolfen N, Albouy
G. Sleeping on the motor engram: the multifaceted nature of
sleep-related motor memory consolidation. Neurosci Biobe-
hav Rev. 2017;80:1-22. doi
11. Pan SC, Rickard TC. Sleep and motor learning: is there
room for consolidation? Psychol Bull. 2015;141(4):812-34.
doi
12. Christova M, Aftenberger H, Nardone R, Gallasch E. Adult
gross motor learning and sleep: is there a mutual benet?
Neural Plast. 2018;2018:1-12. doi
13. Siengsukon CF, Boyd LA. Does sleep promote motor lear-
ning? Implications for physical rehabilitation. Phys Ther.
2009;89(4):370-83. doi
14. Blischke K, Erlacher D, Kresin H, Brueckner S, Malangré
A. Benets of sleep in motor learning - prospects and limi-
tations. J Hum Kinet. 2008;20(2008):23-35. doi
15. Kuriyama K. Sleep-dependent learning and motor-skill
complexity. Learn Mem. 2004;11(6):705-13. doi
16. Malangré A, Blischke K. Sleep-related ofine improve-
ments in gross motor task performance occur under free
recall requirements. Front Hum Neurosci. 2016;10(134):1-
8. doi
17. Al-Sharman A, Siengsukon CF. Sleep enhances learning of
a functional motor task in young adults. Phys Ther. 2013;93
(12):1625-35. doi
18. Gudberg C, Wulff K, Johansen-Berg H. Sleep-dependent
motor memory consolidation in older adults depends on task
demands. Neurobiol Aging. 2015;36(3):1409-16. doi
19. Spencer RMC, Gouw AM, Ivry RB. Age-related decline of
sleep-dependent consolidation. Learn & Mem. 2007;14
(7):480-84. doi
20. Siengsukon CF, Boyd LA. Sleep to learn after stroke: Impli-
cit and explicit off-line motor learning. Neurosci Lett.
2009;451(1):1-5. doi
21. Wulf G, Shea CH. Principles derived from the study of sim-
ple skills do not generalize to complex skill learning. Psy-
chon Bull Rev. 2002;9(2):185-211. doi
22. Genzel L, Quack A, Jäger E, Konrad B, Steiger A, Dresler
M. Complex motor sequence skills prot from sleep. Neu-
ropsychobiology. 2012;66(4):237-43. doi
23. Christina RW. Concerns and issues in studying and asses-
sing motor learning. Meas Phys Educ Exerc Sci. 1997;1
(1):19-38. doi
24. Fischman MG, Christina RW, Vercruyssen MJ. Retention
and transfer of motor skills: a review for the practitioner.
Quest. 1981;33(2):181-94. doi
25. Christina RW, Shea JB. The limitations of generalization
based on restricted information. Res Q Exerc Sport. 1988;59
(4):291-97. doi
26. Oldeld RC. The assessment and analysis of handedness:
the Edinburgh inventory. Neuropsychologia. 1971;9(1):97-
113. http://www.ncbi.nlm.nih.gov/pubmed/5146491
27. Al-Abood SA, Davids K, Bennett SJ, Ashford D, Marin
MM. Effects of manipulating relative and absolute motion
information during observational learning of an aiming task.
J Sports Sci. 2001;19(7):507-20. doi
28. Magill RA, Anderson DI. Motor learning and control: con-
cepts and applications. 11th ed. Dubuque, McGraw-Hill
Education; 2017.
29. Christina RW, Shea JB. More on assessing the retention of
motor learning based on restricted information. Res Q Exerc
Sport. 1993;64(2):217-22. doi
30. Marshall L, Born J. The contribution of sleep to hippo-
campus-dependent memory consolidation. Trends Cogn Sci.
2007;11(10):442-50. doi
31. Kempler L, Richmond JL. Effect of sleep on gross motor
memory. Memory. 2012;20(8):907-14. doi
32. Brawn TP, Fenn KM, Nusbaum HC, Margoliash D. Conso-
lidation of sensorimotor learning during sleep. Learn Mem.
2008;15(11):815-19. doi
33. Malangré A, Leinen P, Blischke K. Sleep-related ofine
learning in a complex arm movement sequence. J Hum
Kinet. 2014;40(1):7-20. doi
34. Lersten KC, Schendel JD, Hagman JD. On sustaining pro-
cedural skills over a prolonged retention interval. J Appl
Psychol. 1982;67(5):418-19. doi
35. Schendel JD, Hagman JD. On sustaining procedural skills
over a prolonged retention interval. J Appl Psychol. 1982;67
(5):605-10. doi
36. Hikosaka O, Nakahara H, Rand MK, Sakai K, Lu X, Naka-
mura K, et al. Parallel neural networks for learning sequen-
tial procedures. Trends Neurosci. 1999;22(10):464-71. doi
37. Hikosaka O, Nakamura K, Sakai K, Nakahara H. Central
mechanisms of motor skill learning. Curr Opin Neurobiol.
2002;12(2):217-22. doi
38. Appleman ER, Albouy G, Doyon J, Cronin-Golomb A,
King BR. Sleep quality inuences subsequent motor skill
acquisition. Behav Neurosci. 2016;130(3):290-7. doi
39. Schmid D, Erlacher D, Klostermann A, Kredel R, Hossner
EJ. Sleep-dependent motor memory consolidation in heal-
thy adults: A meta-analysis. Neurosci Biobehav Rev.
2020;118:270-81. doi
40. King BR, Hoedlmoser K, Hirschauer F, Dolfen N, Albouy
G. Sleeping on the motor engram: the multifaceted nature of
sleep-related motor memory consolidation. Neurosci Biobe-
hav Rev. 2017;80:1-22. doi
Corresponding author
Giordano Marcio Gatinho Bonuzzi, Universidade Estadual
do Piauí, Departamento de Educação Física, Picos, PI,
Brazil.
E-mail: giordanomgb@gmail.com.
Manuscript received on October 29, 2021
Manuscript accepted on May 5, 2022
Motriz. The Journal of Physical Education. UNESP. Rio Claro, SP, Brazil
- eISSN: 1980-6574 - under a license Creative Commons - Version 4.0
6 Sleep and motor learning