Implicit and Explicit Learning of a Sequential Postural Weight-Shifting Task in Young and Older Adults

Abstract

Sequence-specific postural motor learning in a target-directed weight-shifting task in 12 older and 12 young participants was assessed. In the implicit sequence learning condition participants performed a concurrent spatial cognitive task and in the two explicit conditions participants were required to discover the sequence order either with or without the concurrent cognitive task. Participants moved a cursor on the screen from the center location to one of the target locations projected in a semi-circle and back by shifting their center of pressure (CoP) on force plates. During the training the targets appeared in a simple fixed 5-target sequence. Plan-based control (i.e., direction of the CoP displacement in the first part of the target-directed movement) improved by anticipating the sequence order in the implicit condition but not in the explicit dual task condition. Only the young participants were able to use the explicit knowledge of the sequence structure to improve the directional error as indicated by a significant decrease in directional error over practice and an increase in directional error with sequence removal in the explicit single task condition. Time spent in the second part of the movement trajectory to stabilize the cursor on the target location improved over training in both the implicit and explicit sequence learning conditions, for both age groups. These results might indicate that an implicit motor learning method, which holds back explicit awareness of task relevant features, may be desirable for improving plan-based motor control in older adults.

Full text

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ORIGINAL RESEARCH
published: 24 May 2016
doi: 10.3389/fpsyg.2016.00733
Edited by:
Bernard J. Martin,
University of Michigan, USA
Reviewed by:
Luis Augusto Teixeira,
University of São Paulo, Brazil
Rachel O. Coats,
University of Leeds, UK
*Correspondence:
Simone R. Caljouw
s.r.caljouw@umcg.nl
Specialty section:
This article was submitted to
Movement Science and Sport
Psychology,
a section of the journal
Frontiers in Psychology
Received: 04 December 2015
Accepted: 02 May 2016
Published: 24 May 2016
Citation:
Caljouw SR, Veldkamp R
and Lamoth CJC (2016) Implicit
and Explicit Learning of a Sequential
Postural Weight-Shifting Task
in Young and Older Adults.
Front. Psychol. 7:733.
doi: 10.3389/fpsyg.2016.00733
Implicit and Explicit Learning of a
Sequential Postural Weight-Shifting
Task in Young and Older Adults
Simone R. Caljouw*, Renee Veldkamp and Claudine J. C. Lamoth
Center for Human Movement Sciences, University Medical Center Groningen, University of Groningen, Groningen,
Netherlands
Sequence-specific postural motor learning in a target-directed weight-shifting task in
12 older and 12 young participants was assessed. In the implicit sequence learning
condition participants performed a concurrent spatial cognitive task and in the two
explicit conditions participants were required to discover the sequence order either with
or without the concurrent cognitive task. Participants moved a cursor on the screen
from the center location to one of the target locations projected in a semi-circle and
back by shifting their center of pressure (CoP) on force plates. During the training the
targets appeared in a simple fixed 5-target sequence. Plan-based control (i.e., direction
of the CoP displacement in the first part of the target-directed movement) improved by
anticipating the sequence order in the implicit condition but not in the explicit dual task
condition. Only the young participants were able to use the explicit knowledge of the
sequence structure to improve the directional error as indicated by a significant decrease
in directional error over practice and an increase in directional error with sequence
removal in the explicit single task condition. Time spent in the second part of the
movement trajectory to stabilize the cursor on the target location improved over training
in both the implicit and explicit sequence learning conditions, for both age groups. These
results might indicate that an implicit motor learning method, which holds back explicit
awareness of task relevant features, may be desirable for improving plan-based motor
control in older adults.
Keywords: implicit motor learning, postural control, aging, older adults, sequence learning
INTRODUCTION
Repeating patterns or sequences occur often in our environments, and in many activities of daily
living a sequence of individual acts is performed in interaction with the environment. For example,
the sequence of asks needed to get a glass of water may include, leaning over to a cupboard,
opening the cupboard, grasping a glass, moving to the tap, and turning on the faucet. Prediction of,
adaptation to, and learning about, environmental regularities on the basis of preceding events may
assist in how the body needs to be moved in order to achieve the task goal, and requires adequate
postural control (Sturnieks et al., 2008;de Vries et al., 2014).
Aging yields an undeniable deterioration of postural control, as a consequence of a general age-
related deterioration of sensory and neuromuscular control mechanisms (Laughton et al., 2003;
Sturnieks et al., 2008). Consequently, maintaining postural stability during daily tasks becomes
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less automatic, and requires increased attention. Aging, however,
is not only associated with a decline in postural control, but also
with a deterioration of cognitive processes involving executive
functions and attention (Castel and Craik, 2003;Park et al.,
2003;Lovden et al., 2008;Verwey, 2010). Thus, older adults have
greater need for conscious attention to maintain good postural
control, due to impaired sensory and motor system functions. At
the same time, they suffer from reduced attentional and working
memory capacity. Since postural control becomes less automatic,
depending on the complexity of the motor task, the execution of
a concurrent cognitive task will lead to performance decrements
(Huxhold et al., 2006;Boisgontier et al., 2013).
The age-related decline of cognitive functions makes it
plausible that the ability to explicitly learn sequential motor skills
decreases with age, since explicit motor learning requires an
intention to learn and thus a contribution of strategic processes
such as attention, reasoning, and memory (Fitts and Posner,
1967). Young adults acquire more explicit knowledge about the
sequence structure than older adults (Howard and Howard, 2001;
Verneau et al., 2014). When older adults do acquire explicit
knowledge about a sequence, they would be less successful in
using this knowledge (Shea et al., 2006;Verneau et al., 2014).
Implicit learning, on the other hand, is considered to depend on
a phylogenetically older and more primitive system than explicit
learning (Reber, 1992). In implicit learning, learning occurs
without an intention to learn and without explicit knowledge
about the environmental regularities, it thus depends less on the
working memory capacity (Masters, 1992;Jimenez and Vazquez,
2005;Janacsek and Nemeth, 2012). Therefore, it is suggested that
implicit learning is more robust to the effects of age (Cherry and
Stadler, 1995;Song et al., 2009). Abundant research exist on the
influence of age on implicit motor learning used serial reaction
time tasks (Nissen and Bullemer, 1987;Willingham and Goedert-
Eschmann, 1999). In serial reaction time tasks participants have
to react as fast as possible on certain stimuli by pressing keys on
a keyboard, repeating sequences of stimuli are hidden between
random stimuli, in order to remain unknown to the participants
(for reviews see: Rieckmann and Backman, 2009;Howard and
Howard, 2013;King et al., 2013). With practice, participants
become faster due to general skill learning and sequence specific
learning. Sequence-specific learning is indicated by an abrupt
increase in response times when the sequential regularity is
removed. Older adults do show sequence learning in these tasks,
however, the rate and magnitude of learning declines when task
conditions become cognitively more demanding. This occurs
with increased complexity of the sequence due to alternating
random and ordered elements (Curran, 1997;Feeney et al., 2002;
Howard et al., 2004;Bennett et al., 2007;Simon et al., 2011) or due
to an additional working memory load in the form of a dual-task
(Frensch and Miner, 1994;Nejati et al., 2008;King et al., 2013;
Vandenbossche et al., 2014).
In contrast to serial reaction time tasks, taking advantage of
a repeating sequence of elements to improve postural responses
is proven to be difficult. Recent studies (Van Ooteghem et al.,
2008, 2010) question earlier positive findings of Shea et al. (2001)
who showed segment learning in a visuomotor tracking task in
which participants were asked to continuously track a target by
controlling their center of pressure (CoP; moving a platform
on a stabilometer on which they were standing). Chambaron
et al. (2006) suggested that performance improvements in
this previous study were not the result of segment-specific
visuomotor learning, but could be attributed to methodological
flaws, i.e., the selection of a repeating segment that was more
easy to perform than the random control segments. The studies
of Van Ooteghem et al. (2008, 2010) lend further support for
Chambaron et al. (2006) indicating no evidence for sequence
specific learning in a postural control task in which participants
had to maintain balance in response to a repeating pattern of
sequential platform manipulations. On the other hand, Orrell
et al. (2006) showed that application of an implicit motor learning
technique did improve balance performance on a stabilometer.
It is presently not known whether implicit motor learning
would occur for postural control tasks in which participants
produce postural adjustments to environmental regularities
of a sequential nature (instead of reactive to perturbations).
Therefore, in the present study, sequence-specific postural motor
learning in a target-directed weight-shifting task was assessed,
in both older and young participants. Instructing participants
to discover a sequence can attenuate the degree to which
participants gain awareness of the sequence structure, whereas
asking them to concurrently perform a task-irrelevant visuo-
spatial memory task can abolish awareness of the sequence
structure. Previous studies on motor sequence learning in upper
limb tasks indicate that explicit awareness of the sequence order
is a prerequisite for sequence-specific movement optimization
(Moisello et al., 2009, 2011;Oostwoud Wijdenes et al., 2016).
When explicit sequence knowledge is important for sequence-
specific motor learning in a postural task one would expect to find
interference from an added secondary task, especially in older
adults.
In the target-directed weight-shifting task, participants
control their CoP on a force platform by shifting their weight in
order to move a cursor on a screen in front of them (Jongman
et al., 2012;de Vries et al., 2014). Participants are asked to
move the cursor to a target that can appear in one of five
locations. A specific sequence of targets recurs throughout the
practice session. Motor skill in this task requires both adequate
planning and execution. One needs to predict the upcoming
target location to move efficiently to the right side and great
execution skill is required to control the cursor to stabilize
on the target location. The directional accuracy of the CoP
displacement in the first part of the target-directed movement
is a good proxy for the planning accuracy, a higher accuracy
of movement direction reflects better anticipation of the target
location, demonstrating a greater degree of plan-based motor
learning (Ghilardi et al., 2003, 2009). A previous study on
target-directed weight-shifting showed that the steadiness of the
movement increased (i.e., less velocity peaks and dwell time in
the vicinity of the target) when the upcoming target location
was predictable compared to when it was not (Jongman et al.,
2012). This finding suggests that knowledge of the sequence order
and anticipating the target location may improve not only the
initial planning of the target-directed movement (e.g., directional
accuracy in the first part of the movement), but also the visual
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guidance or control over the execution of the movement (e.g.,
homing-time necessary for corrective movements in the vicinity
of the target).
In the current study healthy older and young participants
repeatedly performed a sequence of voluntary displacements
of the CoP to assess whether (1) age affects the capacity for
sequence-specific postural motor learning, (2) explicit knowledge
about the sequence order leads to better movement optimization
than implicit learning, and (3) sequence-specific postural motor
learning degrades under dual task conditions. We hypothesized
that practicing the sequential target-directed weight shifting
task leads to sequence specific improvements in both age
groups. Since the attentional cost of postural control increases
in older adults, we expected also that beneficial effects of
sequence awareness on movement optimization are lower in
older individuals, especially when a cognitive task is performed
simultaneously.
MATERIALS AND METHODS
Participants
Twelve young adults (23.9 ±4.3 years) and 12 older adults
(67.9 ±2.5 years) participated in the experiment. Participants had
no neurological or orthopedic disorders that might have an effect
on cognition or postural control and were able to walk and stand
unaided for at least 1 h. The local institution’s ethical committee
approved the study and the participants signed informed consent.
Apparatus and Task Environment
The experiment was conducted in the Computer Assisted
Rehabilitation Environment laboratory (CAREN; Motek
Medical). Participants stood on two force platforms (Bertec
FP4060-08). On a large screen, positioned 2.5 m in front of
the participant, a cursor provided online feedback of the CoP
displacements of the participant (de Vries et al., 2014). The
displacements of the CoP were displayed on the vertical screen
as cursor movements from left to right for the medio-lateral
component and from top to bottom for the anterior–posterior
component. At the start of the experiment participants stood
in a natural position with arms at the side and the software
positioned the cursor on the center target on the screen goal
targets were presented sequentially in one of five possible
locations on a hemicycle above the central target (north, east,
west, north-east, and north-west). When the cursor touched
the displayed target for 200 ms the target disappeared and
the next target appeared. The distance between the central
target and the radial targets was 72 cm on the screen and the
diameter of the target was 18 cm, this corresponded with a
CoP-displacement of 0.06 and 0.015 m, respectively. Participants
were instructed to move the cursor from the central target to
the appearing radial target and move the cursor back to the
central target when the radial target disappeared and the central
target appeared. They were instructed to make movements
as quickly and as accurately as possible. The participants
were not allowed to move their feet on the force plate. At the
start of the experiment a short training session of 30 radial
targets was performed to familiarize the participants with
the relationship between their body motions and the cursor
displacements.
Design of the Motor Sequence-Learning
Task
In the experimental conditions 20 consecutive blocks were
performed in which the targets were presented either in random
order (4 R-blocks), or in a fixed recurring sequence (16
S-blocks). See Figure 1 for an overview of the series of test
blocks used in each condition. The targets in the R-block were
never presented two times in a row and each target-to-target
movement (e.g., neutral to north, neutral to northwest) was
presented twice. For each condition the first two test blocks of
the experiment were R-blocks consisting of 21 targets. These
random blocks were considered baseline blocks; the first random
block was the random baseline-test (R-Base) and the second
one was used as random pre-test (R-Pre). Subsequently, 15
S-blocks were performed. In each S-block a simple sequence
of five different targets was presented three times. Thus, the
learning phase consisted of 45 sequence repetitions. The sequence
order differed between conditions and participants. The last
sequence block (S15) of this learning phase was used as a
sequence post-test (S-Post). In-between S-block 8 and S-block
9 a break was introduced to allow for a short-term recovery of
fatig. To analyse the effect of sequence removal after sequence
learning, S-Post was followed by a R-block of 21 targets (R-
Post). After R-Post the sequence was reintroduced in block S16
(S-rec), to reveal if sequence learning was retained after the
interfering introduction of a random phase. To diminish effects
of sequence expectation, the sequence was reintroduced without
any warning and immediately followed by another R-block. (R4).
This final R-block was also introduced to prevent participants
from obtaining sequence knowledge in retrospect by re-enacting
the last trials that were performed.
The Learning Conditions
Each participant performed this series of blocks three times
with different instructions. The order of the conditions was
counterbalanced across participants and a rest time of at
least 15 min was introduced between learning conditions. In
the explicit single-task condition participants were instructed
to discover the sequence in the task. In the explicit dual-
task condition participants were instructed to discover the
sequence in the learning phase and were required to perform a
concurrent visuo-spatial memory task. In the implicit condition
the participants were instructed that the targets appeared
in random order throughout this session and performed a
concurrent visuo-spatial memory task. An implicit single-
task condition was not included in the current experiment
since pilot studies showed that young participants became
easily aware of the sequence when the cognitive task was
absent.
The visuo-spatial memory task was an adaptation of the
Brooks Spatial Matrix task (Brooks, 1967). Participants listened to
a set of sentences composing a description of a spatial sequence
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FIGURE 1 | Description of the experimental setup. R, random block; S, Sequence block.
of locations, such as “In the starting square put a 1, in the next
square to the left put a 2, in the next square down put a 3.” For
the younger participants, recorded instructions were given for
number placement after every 10 target-directed movements, for
a total of 17 numbers. Older participants were given instructions
after every 13 target-directed movement and were required to
remember 13 numbers. This task was administered at the start
of the experiment and twice per learning condition (e.g., before
and after the break).
After each learning condition it was tested with a free recall
test whether the participants acquired awareness of the target
sequence. If participants were not able to correctly report the
sequence order a four-way forced-choice test was conducted,
to test sequence recognition. Prior to the experiment two
criteria were formulated regarding the sequence awareness in
the different conditions, (1) participants should become aware
of the sequence in the explicit single-task condition and (2)
participants should not become aware of the sequence in the
implicit condition. Participants were excluded from the data
analysis when they did not meet these criteria.
Data Analysis
Before determining the outcome measures from the CoP
coordinates the raw CoP position data were filtered using a low-
pass fourth order Butterworth filter, with a cut-off frequency of
5 Hz. Subsequently, plan-based and on line control processes
were isolated with a trajectory analysis of each target-directed
FIGURE 2 | Illustration of the center-out movement to a presented
radial target (white) and the outcome parameters directional error and
homing time. The figure is based on one trial of a young subject at the start
(A) and at the end (B) of a practice session. The angle (α) between the two
blue lines determines the directional error. The homing time is the time it takes
from leaving the dotted circle to stabilizing on the radial target (red trajectory).
At the start of the experiment the subject had a larger homing time and a
larger directional error than at the end of the practice session (left panel vs.
right panel).
movement (see Figure 2). Specifically, the directional error of
the first part of the CoP trajectory and the time it takes to
reach and stabilize on the radial target in the second part
(homing-time) of the CoP trajectory were selected to reflect
the plan-based and on-line control processes, respectively. The
directional error was determined at the point where the cursor
leaves the central target area (e.g., the exit point) and defined
as the angle between two lines; one line connecting the exit
point with the origin of the central target and the other
representing the ideal path connecting the origins of the central
target and the radial target. The homing time is the time it
takes from the exit point until the disappearance of the radial
target.
The transition from the sequence posttest (block S15; S-Post)
to the random posttest (R3; R-Post) resulted in large movement
errors on the first trial of the random block. This error was
possibly the result of learning the sequence, causing participants
to wrongly predict an upcoming target location in the random
target location condition. Therefore, the first trial of the 21
trials of the random posttest (block R3) has been removed from
analysis. We excluded from further analysis also the trials in
which the cursor traveled a distance less than 0.01 m in the
home area (6.14% due to technical difficulties) and trials in which
movement times were longer than 2.3 s (0.86%).
Statistical Analysis
All statistical analyses were applied to both outcome measures,
homing time and directional error, separately. Preliminary 2
(Age) ×3 (Condition) repeated-measures ANOVAs with Age
as the between-subjects factor and Condition as the within-
subjects factor were applied to the performance measures in
the random baseline-test (R-Base) to compare the initial task
performance of the young and older participants for the three
conditions. To assess the general training effects over the
sequence blocks, Age (young vs. old) ×Condition (implicit vs.
explicit single vs. explicit dual task) ×Test block (R-Pre vs.
S-post) ANOVAs were applied. To examine whether sequence-
specific learning occurred, sequence removal and sequence
reintroduction effects were tested with Test block (S-Post vs.
R-Post vs. S-Rec) ×Condition (explicit single task vs. explicit
dual-task vs. implicit) ×Age (young vs. old) ANOVAs. To
further explore significant effects, we performed post hoc tests
with Bonferroni corrected adjustments to protect the level of
significance.
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RESULTS
Explicit Knowledge Assessment
In the explicit single-task condition participants were instructed
to discover the sequence while performing the target-directed
weight-shifting task. Upon completion, one older participant did
not show explicit knowledge of the sequence in both the free-
recall and the forced choice task, thus his results were excluded
from further analysis. All young participants acquired explicit
sequence knowledge in the explicit single-task condition and
successfully reported the sequence order in the free recall test. In
the implicit condition, where sequence knowledge should not be
available to the participants, two young and one older participant
revealed the right sequence in the explicit knowledge assessment
tests. The three participants that discovered the sequence order
in the implicit condition were excluded from further analysis.
After performing the explicit-dual task condition all the young
participants and none of the older participants were able to
recall the sequence. When the older adults without declarative
knowledge of the sequence were given the forced-choice test, four
of them were belatedly able to recognize the sequence order.
Interestingly, not all participants that discovered the sequence
order in the training phase also noticed the recurrence of
the sequence in block S16 (test block: S-rec), because it was
hidden between two random blocks (R-Post and R4). Only six
young and five older participants reported that they noticed the
recurrence of the sequence in the explicit single-task condition.
Three young and two older participants mentioned the sequence
recurrence in the explicit dual-task condition and none of the
participants noticed the sequence recurrence in the implicit
learning condition.
Cognitive Task Performance
During the experiment participants were asked to prioritize
the visuo-spatial memory task over sequence learning. Task
performance on the visuo-spatial memory test during sequence
learning was compared with task performance prior to the
experiment. As expected, no significant decrease in performance
on the cognitive task was observed for both the young and
older participants. When tested prior to the experiment the
young participants performed the visuo-spatial memory task
successfully, that is 17 out of 17 numbers were correctly placed.
Young participants correctly placed an average of 15.8 out of 17
numbers at the end of the dual task conditions (explicit dual task
and implicit condition). The older participants scored an average
of 6.9 out of 13 correct numbers before the intervention, while
this was 6.3 out of 13 at the end of the dual task conditions.
These results imply that participants followed the instructions
and were able to focus on the cognitive-task while performing the
target-directed weight-shifting task.
Baseline Motor Task Performance
Mean and standard deviations of homing-time and directional
error for old and young participants per condition on the first
block of trials with random target order, e.g., R-Base are depicted
in Figure 3. A significant main effect of Age was found for
homing-time [F(1,18) =10.22, p=0.005], with a longer homing-
time for the old than the young participants. No significant main
effect of Age was found for directional error. No significant main
effects of Condition nor significant interaction effects of Age by
Condition were revealed, indicating no significant performance
difference between the various conditions at the start of the
experiment.
Practice Phase (R-Pre vs. S-Post)
Mean and standard deviations of homing-time and directional
error for old and young participants per condition on the test
moments R-Pre and S-post are presented in Figure 3.
For homing-time, significant main effects of Age
[F(1,18) =17.55, p=0.001] and Test block [F(1,18) =34.25,
p<0.001] were found. Homing-time was shorter for the young
than for the old participants and performance improved with
practice in all learning conditions, indicated by a decrease in
homing-time. No significant main effect of Condition and no
interaction effects were found.
For directional error, a significant main effect of Test block
[F(1,18) =14.40, p=0.001] and a significant interaction
effect of Test block by Condition [F(2,36) =5.34, p=0.009]
was found. No significant main effect of Age was found. To
assess the difference between R-pre and S-post for each learning
condition separately, post hoc paired t-tests were performed with
an adjusted alpha of 0.017 to protect the level of significance.
Performance improvement over practice was revealed, indicated
by a significant decrease in directional error, in the explicit single
task condition [t(19) =4.13, p=0.001] and in the implicit
condition [t(19) =2.85, p=0.010], but not in the explicit dual
task condition.
Sequence Removal and Sequence
Recurrence Analysis (S-Post vs. R-Post
vs. S-Rec)
Means and standard deviations of homing-time and directional
error for old and young participants per condition on the test
moments S-Post, R-Post, and S-Rec are presented in Figure 3.
For homing-time, a significant main effect of Age
[F(1,18) =16.23, p=0.001] and a significant main effect of Test
block (S-Post, R-Post, S-Rec) was observed [F(2,36) =34.36,
p<0.001]. No significant main effect of Condition and no
significant interaction effects were found. Post hoc pairwise
comparisons with Bonferroni adjustments revealed that homing-
time significantly increased in R-Post compared to S-Post
(p<0.001) and then significantly decreased in S-Rec compared
to R-Post (p<0.001). The homing time was not significantly
different between the test blocks S-Post and S-Rec (p=0.072).
This implies that both young and older adults were able to
improve the time it takes to home in on the target by taking
advantage of the sequence structure, as indicated by a significant
increase in homing-time when the sequence is removed and a
decrease again when the sequence is reintroduced.
For directional error, significant main effects of Test block (S-
Post, R-Post, S-Rec); [F(2,36) =28.29, p<0.001) and Condition
[F(2,36) =3.51, p=0.040] were found. Furthermore, there
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FIGURE 3 | Mean value and standard-error bar for each age group on each test block showing; the absence of an aging effect at the beginning of the
experiment for directional error, a slower homing-time for the older participants, general practice effects on directional error and homing-time
(R-Pre vs. S-Post), and the effects of sequence removal and re-introduction (the phase between the two vertical dotted lines on the right side).
was a significant interaction between Test block and Condition
[F(4,72) =6.80, p<0.001] and also a significant interaction
between Age, Test block, and Condition [F(4,72) =3.09,
p=0.021]. To assess the difference between S-post and R-post
for each learning condition and age group separately, post hoc
pairwise comparisons were performed with a Bonferroni adjusted
alpha of 0.008 to protect the level of significance. For the
older participants a significantly higher directional error with
sequence removal was only observed in the implicit condition
and not in both explicit conditions. For the young participants a
significantly higher directional error with sequence removal was
observed in the implicit and explicit single task conditions but
not in the explicit dual task condition. To further explore the
robustness of the sequence learning effect, differences between
the two sequence blocks (S-post and S-rec) were assessed. In
the implicit condition the difference in directional error between
S-post and S-rec was not significant for both young and older
adults, indicating a robust sequence learning effect. Only for the
young adults in the explicit single task condition a significant
increase in directional error was observed in S-rec compared to
S-post (p<0.001), suggesting an interfering effect of the random
block (R-post), which was inserted between the two sequence
blocks (S-post and S-rec).
DISCUSSION
The aim of the current study was to examine the possible effect(s)
of implicit and explicit learning of a sequential postural task in
older adults compared to young adults. To this end, a target-
directed weight-shifting task was created in a virtual environment
in which targets were presented in a certain sequence or
randomly.
The results showed that participants were able to discover the
simple deterministic sequence order of five targets in the explicit
learning condition. In the implicit condition the concurrent
cognitive task prevented most participants from discovering the
simple sequence, as intended. In accordance with our hypothesis,
and in contrast to previous research using a postural perturbation
task (Van Ooteghem et al., 2008, 2010), we found evidence
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for sequence-specific postural motor learning. With practice
on the sequence blocks young and older participants showed
improved performance and an abrupt decrease in performance
when the sequential regularity was removed. However, depending
on age plan-based motor sequence learning, quantified by
improvements in directional error, was not optimal in all
learning conditions. Conversely sequence specific improvements
in homing time occurred in all participants regardless of learning
condition and age. The general observation that old and young
participants show sequence specific motor learning in a postural
control task is in contrast with the work of Van Ooteghem
et al. (2008, 2010). In a postural motor learning study in which
participants were exposed to a repeated sequence of platform
motions, sequence learning did not occur. Participants improved
with practice, but learning was not better for the repeating
sequence than for the random sequence (Van Ooteghem et al.,
2008, 2010). It should be noted that in our study the task
setup was different, instead of reacting to external perturbations,
participants generated active postural responses to aim for
visually presented targets in a sequential order and showed
sequence specific postural motor learning.
Adding explicit knowledge of the sequence order was not
a prerequisite for acquiring sequence-specific improvements
in target-directed weight-shifting. In both age groups in the
implicit condition, where explicit knowledge of the sequence
order was not acquired, homing time and directional error
improved during prolonged sequence practice. Subsequently,
after practice, homing time and directional error increased with
sequence removal (in test block R-post) and decreased again with
sequence reintroduction (in test block S-rec). This implies that
without knowledge of the sequence order and when distracted
by a cognitive task (in the implicit condition), both older and
young participants showed sequence-specific improvements in
the steadiness of the movement execution and in plan-based
control.
For improving plan-based control (directional error), explicit
information about the sequence order through self-discovery,
was in certain circumstances even detrimental. Participants who
intended to search for the sequence order and concurrently
performed the visuo-spatial cognitive task, did not improve
in directional error. Thus, our hypothesis that a concurrent
cognitive task disrupts postural sequence learning with less
interference on implicit than explicit motor learning was
supported for learning to control the direction of the initial part
of the target-directed movement. Studies using the serial reaction
time task found similar results; explicitly searching for a sequence
structure could disrupt motor sequence learning in conditions in
which there is not sufficient cognitive capacity available (Curran,
1997;Fletcher et al., 2005;Jimenez and Vazquez, 2005). The
multiple explicit requirements of the explicit dual task condition
is likely to have placed a high load on the processing limitations
of the working memory system, thereby retarding improvements
in the advance planning of the upcoming target-directed postural
movement in both young and older participants.
Sequence-specific improvements in the homing time occurred
in both older and young participants regardless of the learning
condition. Thus motor learning in the homing phase was
preserved when the cognitive capacity was overloaded by the
explicit attempts to acquire the sequence order in combination
with performing the visuo-spatial cognitive task. Therefore, it
can be assumed that changes in the homing phase are implicitly
achieved, unmolested by acquiring explicit sequence knowledge
and without much dependence on working memory (Willingham
and Goedert-Eschmann, 1999;Willingham et al., 2002).
Age-related difficulties with sequential motor learning were
observed for plan-based control (directional error) in the explicit
single task condition. Both young and older participants acquired
knowledge of the sequence order in this learning condition,
but only the young participants and not the older participants
showed sequence-specific improvements in directional error, as
revealed by the significant increase in directional error with
sequence removal (in test block R-post). However, for the young
participants, this sequence specific learning was less robust
compared to the implicit condition. This was evidenced by the
fact that reintroducing the sequence unbeknownst to participants
(in test block S-Rec) did not significantly decrease directional
error. Even though explicit knowledge was acquired, one did
not recover from the increase in directional error due to the
random block interference (in test block R-Post). Possibly one
needs to be fully aware of the recurrence of the sequence
before being able to express explicit sequence learning in plan-
based control of the movement (Willingham and Goedert-
Eschmann, 1999). In contrast, in the implicit condition plan-
based control improved (decrease in directional error) when the
sequence was reintroduced (in test block S-Rec). This indicates
a robust implicit memory of the sequence and the ability to
more accurately execute the initial part of the target-directed
movement without sequence awareness. The finding that, for
the older participants, sequence specific learning of directional
error occurred in the implicit condition and not in both explicit
conditions, supports the proposition that implicit motor learning
is relatively preserved with age in comparison with explicit
learning (Reber, 1992;Cherry and Stadler, 1995;Hedden and
Gabrieli, 2004;Shea et al., 2006;Brown et al., 2009;Gaillard et al.,
2009;Song et al., 2009).
A new finding of our work is that sequence practice not
only affects the initial plan-based part of the movement, but
also led to a progressive improvement of motor control late
in the movement trajectory in both young and older adults.
Successful achievement of the task goal depends not only on
correctly anticipating the target and planning a movement
with the right direction and extent, but also on the ability to
quickly adjust the ongoing movement based on visual feedback
about the effector and target (Glover, 2004;Caljouw et al.,
2006, 2011). When sequential arm-reaching movements are
practiced, control shifts from a reaction mode to an anticipatory
mode within a few practice trials, requiring far less online
visual control at the end of the practice session than at the
start of the practice session (Ghilardi et al., 2003, 2009). In
our target-directed weight-shifting task, the target area is not
easily reached given the inherent variability in postural control,
which is observed even during quiet standing in the start
position (Zatsiorsky and Duarte, 2000;Lamoth et al., 2009).
Even after practice, a directional error with a large standard
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Caljouw et al. Learning Sequential Postural Weight-Shifting
deviation was still present. The presence of a directional error
highlights the need for corrections in the vicinity of the target
area, to achieve a rather stable final position within the target.
The homing time in older participants was substantially longer
than young participants, indicating less optimal control in the
vicinity of the target (Jongman et al., 2012;de Vries et al.,
2014). Despite this difference in performance, both older and
younger participants showed changes in homing time with
sequence removal and reintroduction after practice, indicating
age-invariant sequence-specific performance optimization late in
the movement trajectory.
Participants showed a progressive improvement in aim
direction and homing time for the sequence elements without
explicit awareness of the sequence in the implicit condition.
This is inconsistent with previous work on upper-limb motor
sequence learning suggesting that sequence awareness allows for
a progressive change in movement execution (Moisello et al.,
2009, 2011;Oostwoud Wijdenes et al., 2016). For example, in a
finger-opposition task procedural optimization of the movement
(reflected by a change in thumb-finger touch duration) was
reached only in conditions in which participants acquired explicit
sequence knowledge (Moisello et al., 2011). The observations
in our study do not support the suggestion that knowledge is
important for motor learning (Stanley and Krakauer, 2013;Wong
et al., 2015).
CONCLUSION
The results of the present study show that sequence learning in a
postural visuomotor control task is possible in both young and
older adults. The most robust learning effects for both groups
were observed for the implicit learning condition. Only the young
participants were able to decrease the directional error with
sequence practice in the explicit condition, implying that older
adults were hampered by the additional attentional cost of explicit
sequence monitoring. In contrast, focusing attention on task-
irrelevant aspects during sequence practice (i.e., the cognitive
task in the implicit condition) did not hamper improvement
in both aim direction and homing time in older adults. The
finding that introducing a secondary task that prevented the
accumulation of explicit knowledge resulted in a robust learning
effect provides further support for the notion that implicit motor
learning methods may be desirable for older adults.
AUTHOR CONTRIBUTIONS
SC and CL made substantial contributions to conception and
design, acquisition of data, and analysis and interpretation
of data. RV made substantial contribution to analysis and
interpretation of data. SC, CL, and RV participated in drafting the
article and revising it critically for important intellectual content;
and give final approval of the version to be submitted and are
accountable for all aspects of the work in ensuring that questions
related to the accuracy or integrity of any part of the work are
appropriately investigated and resolved.
ACKNOWLEDGMENT
We thank Sander Woldhek for the data collection and Helco van
Keeken for programming the Computer Assisted Rehabilitation
Environment.
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Conflict of Interest Statement: The authors declare that the research was
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