J Neurophysiol 114: 419 – 426, 2015.
First published April 29, 2015; doi:10.1152/jn.00222.2015.
Accessory stimulus modulates executive function during stepping task
Tatsunori Watanabe,1 Soichiro Koyama,2 Shigeo Tanabe,3 and Ippei Nojima1
1
Department of Physical Therapy, Graduate School of Medicine, Nagoya University, Aichi, Japan; 2Department of
Rehabilitation, Kawamura Hospital, Gifu, Japan; and 3Faculty of Rehabilitation, School of Health Sciences, Fujita Health
University, Aichi, Japan
Submitted 9 March 2015; accepted in final form 28 April 2015
judgment; inhibition; postural control; accessory stimulus; executive
function
TAKING A QUICK CORRECT STEP response while inhibiting an
incorrect one to environmental stimuli is a fundamental human
function, and failing to do so potentially leads to falls. Findings
from previous studies revealed that falls were associated with
delayed step initiation caused by increased demands of attention (Lord and Fitzpatrick 2001; Pijnappels et al. 2010; St
George et al. 2007). Most previous studies, however, examined
the stepping behavior using only one sensory modality, even
though in reality humans receive information simultaneously
from multiple sensory modalities. Moreover, the control of
balance and posture in fall prevention is a complicated central
sensorimotor function that integrates information from visual,
vestibular, and somatosensory systems. Thus, to advance our
understanding of the control of gait initiation and falls associ-
Address for reprint requests and other correspondence: I. Nojima, Dept. of
Physical Therapy, Nagoya Univ. Graduate School of Medicine, 1-1-20 DaikoMinami, Higashi-ku, Nagoya-shi, Aichi 461-8673, Japan (e-mail: nojima
@met.nagoya-u.ac.jp).
www.jn.org
ated with it, it is necessary to investigate such executive
functions as stimulus identification, response selection, and
postural preparations during stepping movement in the context
of multisensory integration.
Reaction time (RT), commonly measured in simple reaction
time (SRT) and choice reaction time (CRT) paradigms, can be
reduced when multiple modalities simultaneously present the
stimuli. Acoustic stimuli presented at nearly the same time as
a visual imperative stimulus can reduce RTs, and these facilitation effects were found with both startling and nonstartling
accessory stimuli (Carlsen et al. 2004a, 2004b; Hackley and
Valle-Inclán 1998, 1999; Valls-Solé et al. 1995, 1999). Regarding stepping, gait initiation, or walking, however, most
previous studies presented RT reduction mainly with startling
acoustic stimuli and relatively simple tasks (MacKinnon et al.
2007; Queralt et al. 2008, 2010; Reynolds and Day 2007). Thus
clarifying the effects of accessory stimuli on RTs in complex
stepping movements would inform us about the intersensory
judgment processes during such movement.
Along with RT reduction, acoustic stimuli are reported to
enlarge the interference effect in a Simon task (Böckler et al.
2011; Fischer et al. 2010; Soutschek et al. 2013), in which
responses are made according to the direction (not the location)
of an arrow that is presented to either the right or the left of a
central fixation (Simon 1969). In addition, they can cause an
increase in the error rates in CRT tasks (Carlsen et al. 2004a;
Low et al. 1996; Schmidt et al. 1984). However, previous
multisensory studies investigated only overt errors. Partial
errors can be observed, prior to the correct response, in electromyographic activity of the side that is associated with the
incorrect responses (Burle et al. 2002, 2008; Masaki et al.
2012; Vidal et al. 2000). A similar phenomenon has recently
been found in stepping reaction. Errors in the initial weight
transfer of the postural responses prior to a step [i.e., anticipatory postural adjustment (APA) errors], indicative of motor
program errors, may occur when the direction of a stepping
movement is not known in advance, and arguably inhibitory
control is related to those APA errors (Cohen et al. 2011;
Sparto et al. 2013, 2014; Uemura et al. 2013a, 2013b). These
previous studies hence propose that motor programming possibly deteriorates further in the presence of acoustic stimuli.
Thus it is important to examine stepping reactions to stimuli
from multiple sensory modalities, as information from multiple
sensory modalities is more indicative of everyday experience.
In this study, we presented the visual imperative and acoustic accessory stimuli simultaneously, using the Simon task
because this task affects only premotor time while the flanker
task (another response compatibility task used commonly in
RT paradigms) affects both premotor time and motor time to
0022-3077/15 Copyright © 2015 the American Physiological Society
419
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Watanabe T, Koyama S, Tanabe S, Nojima I. Accessory stimulus modulates executive function during stepping task. J Neurophysiol 114: 419 – 426, 2015. First published April 29, 2015;
doi:10.1152/jn.00222.2015.—When multiple sensory modalities are
simultaneously presented, reaction time can be reduced while interference enlarges. The purpose of this research was to examine the
effects of task-irrelevant acoustic accessory stimuli simultaneously
presented with visual imperative stimuli on executive function during
stepping. Executive functions were assessed by analyzing temporal
events and errors in the initial weight transfer of the postural responses prior to a step (anticipatory postural adjustment errors).
Eleven healthy young adults stepped forward in response to a visual
stimulus. We applied a choice reaction time task and the Simon task,
which consisted of congruent and incongruent conditions. Accessory
stimuli were randomly presented with the visual stimuli. Compared
with trials without accessory stimuli, the anticipatory postural adjustment error rates were higher in trials with accessory stimuli in the
incongruent condition and the reaction times were shorter in trials
with accessory stimuli in all the task conditions. Analyses after
division of trials according to whether anticipatory postural adjustment error occurred or not revealed that the reaction times of trials
with anticipatory postural adjustment errors were reduced more than
those of trials without anticipatory postural adjustment errors in the
incongruent condition. These results suggest that accessory stimuli
modulate the initial motor programming of stepping by lowering
decision threshold and exclusively under spatial incompatibility facilitate automatic response activation. The present findings advance the
knowledge of intersensory judgment processes during stepping and
may aid in the development of intervention and evaluation tools for
individuals at risk of falls.
420
ACCESSORY STIMULUS AND EXECUTIVE FUNCTION
METHODS
Participants. Eleven participants (5 men, 6 women; mean ⫾ SD
age ⫽ 22 ⫾ 2.24 yr) without a history of hearing, neurological, or
orthopedic disorders that could influence the balance function were
recruited from Nagoya University School of Health Sciences. All
participants had normal or corrected-to-normal vision. The study was
approved by the Ethics Committee of Nagoya University, and written
informed consent was obtained before participation.
Apparatus and procedures. Participants were required to maintain
a stationary standing posture on a force plate (Tec Gihan, Kyoto,
Japan) with their bare feet and stepped forward in response to a visual
imperative stimulus that appeared on a computer screen set just below
eye level at a 1.0-m distance from the participant. Acoustic accessory
stimuli (1,000 Hz, 80 dB) were also delivered randomly and simultaneously with the visual stimuli from two speakers, one placed on
each side of the monitor. Visual and acoustic stimulus generation and
signal acquisition were performed in customized LabVIEW programs
(National Instruments, Austin, TX).
The initial standing position was the same for all participants; each
foot was placed 5 cm apart from a center line drawn vertically to the
frontal plane on the force plate. Forward stepping distance was also
determined to be 45% of the participant’s leg length, measured from
the greater trochanter to the floor. Before each trial, they were
instructed to balance the weight of their feet evenly, which was
confirmed by the position of the center of pressure (COP) obtained
online from the force plate. The visual stimulus was an arrow (⬍ or
⬎) appearing on either the right or left side of the fixation point on the
computer screen, and the participant stepped forward with the leg that
corresponded to the direction of an arrow (⬍ was assigned to the left
leg and ⬎ was assigned to the right leg) onto a wood plate placed right
front of the force plate and brought the other leg alongside. Participants were instructed to execute the movement as quickly and accurately as possible, and after the stepping they were required to move
back to the same starting position and prepare for the next trial.
Stimuli and tasks. The protocol for the presentation of visual and
acoustic stimuli was the following: the fixation point (black plus
shape) was displayed at the center of a white computer screen for
9,500 ms, which was followed by a visual imperative stimulus of a
black arrow (500 ms long) and a randomly presented acoustic accessory stimulus (300 ms long). Thus the total presentation time for each
trial was 10 s.
Each participant performed two blocks of the CRT task and four
blocks of the Simon task (Fig. 1). For all blocks, acoustic accessory
stimuli were presented randomly in 50% of the trials. In the CRT task,
a right-pointing arrow on the right side and a left-pointing arrow on
the left side of the monitor were displayed randomly. Each CRT block
consisted of 20 trials in total, with 10 right-pointing and 10 leftpointing arrows. In the Simon task, cues indicating the step direction
were congruent (⬍ on the left side, ⬎ on the right side) or incongruent
(⬍ on the right side, ⬎ on the left side) and all stimuli were presented
pseudorandomly. Each Simon block consisted of 40 trials in total,
with 20 congruent and 20 incongruent trials. Since the location and
direction of the arrows did not match during incongruent trials, the
participant was required to inhibit the response toward the location of
the arrows.
Data collection and analysis. The data of ground reaction forces
during step executions were collected with a force plate at a sampling
rate of 1,000 Hz, and several temporal parameters were identified
off-line with programs written in MATLAB (MathWorks, Natick,
MA). The obtained mediolateral COP data were low-pass filtered at a
cutoff frequency of 50 Hz with a fourth-order zero-phase lag Butterworth filter, and the baseline was defined as the mean value over the
period from ⫺500 ms to 0 ms with respect to the imperative visual
stimulus. All subsequent procedures were similar to previous studies
(Melzer and Oddsson 2004). The following parameters were extracted
from step execution data (Fig. 2A). The RT was detected as the time
at which the COP deviated mediolaterally toward either the swing or
stance leg for at least 4 mm from the baseline. Foot-lift time was
detected as the time at which the mediolateral shift of the COP toward
the stance leg ended (when the speed of the COP movement toward
the stance leg becomes ⬍100 mm/s twice in row). In addition, the
time from the RT to foot-lift time was defined as APA duration. APA
errors were identified by the first mediolateral deviation of COP
toward the stance leg for at least 4 mm from the baseline, indicating
the presence of two or more postural adjustments before the final
mediolateral shift toward the stance leg in one step execution (e.g.,
COP shifted to the stance leg first and then to the swing leg, which
was followed by the final COP shift to the stance leg) (Fig. 2B).
Statistical analysis. Prior to data analyses of the trials, trials in
which 1) RTs were faster than 3 SD below the mean of each block
(i.e., guessed response), 2) RTs were slower than 3 SD above the
mean of each block (i.e., overthought response), 3) mediolateral sway
was ⬎4 mm during the baseline period, or 4) participants stepped with
the wrong foot or failed to step were excluded. Additionally, before
calculation of overall APA error rate, RT, APA duration, and foot-lift
time, left and right steps were combined, since the mean RT, APA
duration, and foot-lift times were confirmed not to be different (CRT:
P ⫽ 0.47 for RT, P ⫽ 0.28 for APA duration, P ⫽ 0.21 for foot-lift
Choice Reaction Time
>
Block 1-2
<
Simon (congruent and incongruent)
>
<
Block 3-6
>
<
Fig. 1. Visual imperative stimuli used in each block. Choice reaction time task
consisted of both a right arrow on the right side and a left arrow on the left side.
The Simon task comprised congruent (a right arrow on the right side or a left
arrow on the left side) and incongruent (a right arrow on the left side or a left
arrow on the right side) conditions.
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the overall RT (Eriksen et al. 1985; Hasbroucq et al. 1999).
This means that the effects of acoustic accessory stimuli on RT
could be examined without considering the task specificity
with the Simon task. In addition, we applied the CRT task to
examine whether task difficulty plays any role.
The purpose of the present research was to examine the
effects of acoustic accessory stimuli simultaneously presented
with visual stimuli on executive functions during forward
choice stepping. We hypothesized that if an acoustic accessory
stimulus influences stimulus identification and response selection as stated during step execution, then the APA error rate of
trials with accessory stimuli would be higher than that of trials
without accessory stimuli in CRT and Simon tasks, most
notably in the incongruent condition (i.e., mismatch of the
direction and location of the visual imperative stimuli) of the
Simon task. Furthermore, RT of trials with accessory stimuli
were hypothesized to be shorter than trials without accessory
stimuli in CRT and Simon tasks. In addition, movement times
after reacting to a stimulus were hypothesized to be lengthened
by accessory stimuli, since accessory stimuli can increase
response force (Kiesel and Miller 2007; Miller et al. 1999;
Stahl and Rammsayer 2005).
ACCESSORY STIMULUS AND EXECUTIVE FUNCTION
COPx (mm)
Foot-lift
50
RT
0
C
- 50
APA duration
Foot-lift
50
0
C
RT
- 50
0
0.5
1.0
Time (seconds)
Fig. 2. Examples of force plate data for forward step execution with the right
leg. A: no-anticipatory postural adjustment (APA)-error trial. B: APA-error
trial. Vertical line represents mediolateral center of pressure (COPx), and
timing of the visual imperative stimulus is indicated by C. Reaction time (RT)
and foot-lift time were extracted from the data. APA duration was calculated
as the time from RT to foot-lift time. The APA error can be identified by the
initial incorrect COPx shift toward the stance leg. See text for details.
time; Simon task: P ⫽ 0.87 for RT, P ⫽ 0.64 for APA duration, P ⫽
0.67 for foot-lift time). All statistical analyses were performed with
SPSS (IBM, Armonk, NY), and ␣ level was set at P ⬍ 0.05 for all
tests.
First, two-way repeated-measures analysis of variance (ANOVA)
was conducted to determine the effects of acoustic accessory stimuli
and task conditions on APA errors. Since many of our analyses
consisted of different numbers of trials in each cell depending on the
task condition and the presence or absence of an APA error, we used
a linear mixed model for all subsequent analyses. The effect of
accessory stimuli and task conditions on RT, APA duration, and
foot-lift time was examined with sound (off and on) and condition
(CRT, congruent, and incongruent) as fixed factors and participant as
a random factor. Next, to determine the effect of APA errors as well
as acoustic accessory stimulus with respect to the presence or absence
of APA errors on RT, APA duration, and foot-lift time, we constructed a series of linear mixed models with each of those temporal
parameters (RT, APA duration, and foot-lift time) as dependent
variables, APA error (present and absence) and sound (off and on) as
fixed factors, and participant as a random factor. These models were
administered for each of the task conditions. Bonferroni post hoc
analyses were performed to test interaction effects and to determine
the locus of the difference.
RESULTS
Anticipatory postural adjustment error rate. Each participant completed 40 trials of the CRT task and 160 trials of the
Simon task. Thus there were a total of 440 trials of the CRT
task and 1,760 trials of the Simon task (880 trials of the
congruent condition and 880 trials of the incongruent condition). The total number of trials that were analyzed in this study
was 2,131 (3.1% excluded). Figure 3 shows the changes in
APA error rates for sound-off and sound-on trials in each
80
sound off
sound on
60
40
20
0
CRT
CON
Condition
*
INC
Fig. 3. Mean APA error rates for sound-off and sound-on trials obtained from
all participants in 3 different conditions. CRT, choice reaction time; CON,
congruent; INC, incongruent. Error bars show SE. *P ⫽ 0.001 between
sound-off and -on trials.
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COPx (mm)
B
condition. The analyses of the ANOVA revealed the significant
interaction of sound and condition [F(2,20) ⫽ 9.13, P ⫽
0.003]. Post hoc analysis revealed that APA error rates of trials
with sound were significantly higher than trials without sound
in the incongruent condition (P ⫽ 0.001) but not in other
conditions, indicating that the sound’s effect on APA errors
was robust only in the incongruent condition.
Reaction time, anticipatory postural adjustment duration,
and foot lift. The linear mixed model revealed the significant
main effect of sound [F(1,2125) ⫽ 71.67, P ⬍ 0.001] and
condition [F(2,2125) ⫽ 49.92, P ⬍ 0.001] on the RT (Fig. 4A).
Post hoc analysis confirmed that RTs of trials with sound
were significantly shorter than those of trials without sound
in all conditions (P ⬍ 0.001) and that all conditions were
different (P ⬍ 0.001) except for the congruent and incongruent conditions.
An interaction of sound and condition on the APA duration
was significant [F(2,2125) ⫽ 7.09, P ⫽ 0.001] (Fig. 4B). Also,
the main effects of sound [F(1,2125) ⫽ 15.04, P ⬍ 0.001] and
condition [F(2,2125) ⫽ 91.92, P ⬍ 0.001] were revealed. The
interaction of sound and condition can be explained by longer
APA duration in trials with sound compared with trials without
sound only in the incongruent condition (P ⬍ 0.001) and not in
other conditions. This could indicate that sound only affected
the APA durations of the incongruent condition.
An interaction of sound and condition on the foot-lift time
was significant [F(2,2125) ⫽ 6.40, P ⫽ 0.002] (Fig. 4C).
Furthermore, a main effect of condition was found [F(2,2125) ⫽
191.40, P ⬍ 0.001]. Post hoc analysis showed that the foot-lift
times of trials with sound were significantly shorter than those
of trials without sound in CRT (P ⫽ 0.028) and congruent
(P ⫽ 0.016) conditions but not in the incongruent condition,
which potentially resulted from the increased APA duration in
the incongruent condition.
Influence of anticipatory postural adjustment errors on temporal parameters of stepping. The above results indicate that
APA errors and APA durations were affected by accessory
stimuli only in the incongruent condition while RTs were
reduced with accessory stimuli in all conditions. Thus we next
examined the influence of APA errors on the temporal param-
APA error rate (%)
APA duration
A
421
422
ACCESSORY STIMULUS AND EXECUTIVE FUNCTION
A
360
sound off
Reaction Time (ms)
sound on
330
300
0
CON *
INC *
CRT
CON
INC *
460
430
400
370
0
Foot-lift time (ms)
C
780
720
660
0
CRT **
CON **
INC
Condition
Fig. 4. Changes in temporal parameters of step execution for sound-off and -on
trials across all participants in 3 different conditions. A: reaction time. B: APA
duration. C: foot-lift time. Error bars show SE. *P ⬍ 0.001, **P ⬍ 0.05
between sound-off and -on trials.
eters (RT, APA duration, and foot-lift time). Figure 5 shows
the temporal parameters of trials that were divided according to
the presence or absence of APA error and sound.
Figure 5A shows the mean RTs of the divided trials. In the
CRT condition, the analysis of the linear mixed model indicated a significant main effect of sound [F(1,421) ⫽ 22.28,
P ⬍ 0.001] but not a main effect of APA error or their
interaction. In the congruent condition, RT was significantly
affected by sound [F(1,852.09) ⫽ 4.40, P ⫽ 0.036] and APA
errors [F(1,852.06) ⫽ 4.93, P ⫽ 0.027]. In the incongruent
condition, the interaction of sound and APA error was significant [F(1,846.18) ⫽ 6.90, P ⫽ 0.009]. Post hoc analysis
revealed a significant reduction in RT for APA-error trials
(P ⬍ 0.001) but not for non-APA-error trials, suggesting that
DISCUSSION
The present study investigated whether an acoustic accessory stimulus simultaneously presented with a visual imperative stimulus influences the executive functions by increasing
APA errors and reducing RTs during forward choice stepping.
We hypothesized that APA error rates would be greater in trials
with an accessory stimulus for all conditions, particularly in the
incongruent condition of the Simon task, and that the RTs
would be shorter in trials with an accessory stimulus for all
tasks. This hypothesis was partially supported: the RTs were
reduced with accessory stimuli in all conditions as expected;
however, we found that accessory stimuli caused an increase in
the APA error rates only in the incongruent condition. Additionally, we observed that APA durations were increased with
accessory stimuli in the incongruent condition and the foot-lift
times were shortened with accessory stimuli in all but incongruent conditions.
Dividing the trials according to whether APA errors occurred or not further enabled us to interpret the stepping
behavior with accessory stimuli in detail. The imperative
stimulus of an arrow used in the present study has both
directional and locational information. The directional information is the direction that the arrow is pointing to (⬍ for left
and ⬎ for right). The locational information is the side of the
monitor where the arrow is presented (left or right). The
accessory stimuli speeded the response toward both the location and direction of the imperative visual stimulus in the CRT
and congruent conditions, whereas the accessory stimuli affected the response toward the location of the stimulus in the
incongruent condition. This indicates that the accessory stimuli
facilitated automatic response toward the stimulus location
exclusively under spatial incompatibility, as discussed below
in detail.
The APA error rates of conditions without accessory stimuli
obtained in this study were similar to those in previous studies
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APA duration (ms)
B
CRT *
accessory stimuli influenced RT only in the presence of APA
errors in the incongruent condition (Fig. 5A).
Figure 5B provides the mean APA durations of the divided
trials. In the CRT condition, the main effect of APA error was
significant [F(1,420.61) ⫽ 144.29, P ⬍ 0.001] but not the main
effect of sound or their interaction. Likewise, in the congruent
condition, a significant main effect of APA error [F(1,853) ⫽
241.94, P ⬍ 0.001] was revealed but no main effect of sound
or their interaction was present. In the incongruent condition,
a significant interaction between sound and APA error
[F(1,846.04) ⫽ 671, P ⫽ 0.01] was indicated. Post hoc
comparison indicated that the APA durations of the APA-error
trials but not the non-APA-error trials were significantly
lengthened by sound (P ⫽ 0.008).
Figure 5C illustrates the mean foot-lift time of the divided
trials. The main effects of APA error [F(1,420.65) ⫽ 88.32,
P ⬍ 0.001] and sound [F(1,420.08) ⫽ 12.93, P ⬍ 0.001], but
not their interaction, were significant in the CRT condition. In
the congruent condition, a significant main effect of APA error
[F(1,852.01) ⫽ 12.58, P ⬍ 0.001] was present but no main
effect of sound or their interaction. Similarly in the incongruent
condition, the main effect of APA error was significant
[F(1,846.15) ⫽ 116.95, P ⬍ 0.001] but not the main effect of
sound or their interaction.
ACCESSORY STIMULUS AND EXECUTIVE FUNCTION
No APA error
APA error
Reaction time (ms)
370
A
#
##
310
280
sound off
sound on
sound off
sound on ††
sound off*
sound on*
**
B
Fig. 5. Effects of APA error and accessory
stimulus (sound off or on) on temporal parameters of step execution. A: reaction time. B:
APA duration. C: foot-lift time. Data represent
averages of all participants and 3 different
conditions: choice reaction time, congruent,
and incongruent conditions. Error bars show
SE. #P ⬍ 0.001, ##P ⬍ 0.05, main effects for
sound. †P ⬍ 0.001, ††P ⬍ 0.05, main effects
for APA error. *P ⬍ 0.001, **P ⬍ 0.05, post
hoc significance (Bonferroni test).
450
400
350
0
sound off
820
C
sound on †
sound off
sound on†
sound off *
sound on*
sound on †
sound off
sound on †
sound off
sound on †
#
770
720
670
0
sound off
Choice reaction time
Congruent
(Sparto et al. 2013; Uemura et al. 2013b). The present study
revealed that accessory stimuli caused an increase in the APA
error rates only in the incongruent condition (Fig. 3). In
previous studies, overt errors, which are different from the
partial errors that APA errors are considered to be, were
investigated by presenting an accessory stimulus with an imperative visual stimulus in CRT paradigms. However, findings
employing this method have been inconsistent. In some studies
significantly increased overt error rates in the presence of
accessory stimuli were observed (Low et al. 1996; Schmidt et
al. 1984), while other studies showed no significant effect of
accessory stimuli on overt error rates (Hackley and ValleInclán 1999; Jepma et al. 2009).
In regard to this inconsistency, Jepma et al. (2009) proposed
task difficulty as a potential mechanism. In a two-choice
decision process, a decision is made when evidence from
sensory modalities reaches a decision threshold from a starting
point that is set at half the magnitude of two decision thresh-
Incongruent
olds if unbiased. Relatively easy tasks with short RTs (⬍350
ms) have a decision threshold close to the starting point of the
decision process, while more complex tasks with somewhat
longer RTs (⬎500 ms) have a decision threshold at a large
distance from the starting point. Accessory stimuli are suggested to lower a decision threshold in the response selection
process. Thus decisions are unintentionally and incorrectly
made in the presence of accessory stimuli in easy tasks since
the decision threshold is initially set close to the starting point,
while in complex tasks error rates are not heavily influenced by
accessory stimuli (Jepma et al. 2009).
In the present study, although the type of error was
different from that in the previous works, APA error rates
should be increased in the presence of accessory stimuli
when considering the RTs. The obtained results indicated,
however, that accessory stimuli affected the APA error rate
only in the incongruent condition, indicating that the stimulus location may have impacted the outcomes. In studies by
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500
APA duration (ms)
*
340
0
Foot-lift time (ms)
423
424
ACCESSORY STIMULUS AND EXECUTIVE FUNCTION
unintentionally associated with the stimulus location and acted
as a retrieval cue (Steinborn et al. 2009, 2010).
With regard to the APA durations, additional investigations
suggested the possibility that motor execution processes were
affected by accessory stimuli. In all conditions, regardless of
the presence of accessory stimuli, APA durations were lengthened in APA-error trials (Fig. 5B), derived from the additional
mediolateral weight shifts caused by APA errors (Uemura et al.
2013a, 2013b). In the incongruent condition, unlike the other
two conditions, the accessory stimuli lengthened the APA
duration only of APA-error trials. If the lengthened APA
durations in the incongruent condition (shown in Fig. 4B) were
solely caused by the increased APA error rates, then the APA
durations of APA-error trials should not be affected by accessory stimuli. This suggests that accessory stimuli have effects
on the motor execution stage of stepping movement when
responding incorrectly to the stimulus location. However, APA
durations of non-APA-error trials in the CRT and congruent
conditions should have been lengthened by accessory stimuli,
which was not evident in this study. Another possibility is that
accessory stimuli may have hampered the process of noticing
and correcting an incorrect response. Nevertheless, future research will be needed to clarify the mechanisms behind this
phenomenon.
Analysis of foot-lift times with respect to APA errors revealed that accessory stimuli shortened the foot-lift times of
both APA-error and non-APA-error trials in the CRT condition, and a similar tendency was seen in the congruent condition (Fig. 5C). In contrast, the response facilitation that primarily occurred toward the stimulus location as well as lengthened APA durations of APA-error trials in the incongruent
condition reduced the effect of accessory stimuli on foot-lift
time.
Increased APA errors in older individuals compared with
younger adults have been reported. APA errors were considered related to executive function, especially inhibitory control
(Cohen et al. 2011; Sparto et al. 2013, 2014). Furthermore,
increased stepping reaction errors (Schoene et al. 2014) and
delayed step initiation and completion of a voluntary step
(Lord and Fitzpatrick 2001; Pijnappels et al. 2010; St George
et al. 2007) were associated with falls in the elderly. The
presence of an APA error can result in those situations. The
present study broadened our understanding by presenting
sound simultaneously with visual stimuli and revealed that
acoustic accessory stimuli extend the degree of APA errors
when spatial incompatibility is present. Thus it is conceivable
that acoustic sound modulates executive function during stepping, leading to delayed completion of a step and, potentially,
falls. Identifying the effects of aging on this particular matter
may be a future research subject, since older individuals tend to
set decision thresholds differently than younger adults (Forstmann et al. 2011). Moreover, the current fall assessment tools
are not sensitive enough to detect early-stage impairments
(Barry et al. 2014; Schoene et al. 2013). Therefore, the advances on this issue may aid in the development of clinical
measures to identify individuals at risk of falls as well as
prevention programs.
The limitation of the present study would be an extra
cognitive load that was imposed upon the participants when
they were trying to balance the weight of their feet evenly.
Even though it was necessary to avoid a weight distribution on
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Fischer et al. (2010) and Böckler et al. (2011), who investigated the influence of accessory stimuli on the Simon
effect, which is the difference in RT between congruent and
incongruent conditions, results supportive of this prediction
were presented. These studies found a reduction in RTs for
both congruent and incongruent conditions and further
found an increase in the Simon effect as a result of the
accessory stimulus. Fischer et al. (2010) argue that accessory stimuli generally decrease RTs and additionally lower
the decision threshold based on the location of the visual
stimulus regardless of whether the response is correct or not.
This means that in the incongruent condition subjects initially responded based on the stimulus location incorrectly
but to the degree of not making an overt error and later
corrected the response based on the stimulus identity (i.e.,
direction of an arrow) more in trials with accessory stimuli
than in trials without accessory stimuli. However, the previous research failed to examine partial errors that may have
occurred on the side that initially responded incorrectly. In
the present study, it is likely that the same mechanism (i.e.,
facilitation of automatic response activation) occurred, and
an increase in the Simon effect by an accessory stimulus was
indicated alternatively by the increased APA errors.
Beside the interference effect of accessory stimuli, the
present study elucidates the facilitation effect of accessory
stimuli on RTs during a stepping task. In all conditions,
accessory stimuli significantly reduced the RTs (Fig. 4A).
With the statistical analysis of RTs without taking the APA
errors into consideration, however, it is not clear whether
the stimulus location-based facilitation certainly occurred.
In addition, there is a possibility that the lengthened APA
durations in the incongruent condition were induced by the
accessory stimuli affecting the motor execution process
toward the location of the visual stimulus (Kiesel and Miller
2007; Miller et al. 1999; Stahl and Rammsayer 2005),
although they appear to be caused by the increased APA
error rate (Fig. 4B) (Uemura et al. 2013b). This may have
further resulted in the reduction of facilitation effect by
accessory stimuli on foot-lift time in the incongruent condition (Fig. 4C). To clarify the effects of accessory stimuli
on the automatic response activation and thus the APA
errors as well as the motor execution process, we analyzed
the temporal parameters of trials that were divided according to the presence or absence of APA errors.
Additional analysis of RT with respect to APA errors confirmed that accessory stimuli generally lower the decision
threshold irrespective of stimulus type and also lower it based
on the locational information of the visual stimuli under spatial
interference (Fig. 5A), which is consistent with the rationale for
the increased APA error rate. In the CRT condition and the
congruent condition of the Simon task, accessory stimuli reduced the RTs of both APA-error and non-APA-error trials,
implying that the facilitation by accessory stimuli occurs regardless of the visual stimulus location or identity. In contrast,
accessory stimuli reduced the RTs only for APA-error trials in
the incongruent condition. This indicates that accessory stimuli
modulated automatic response activation and reduced the RTs
based on the visual stimulus location when there was a spatial
incompatibility. In addition, the automatic activation of responses implies that accessory stimuli have potentially been
ACCESSORY STIMULUS AND EXECUTIVE FUNCTION
ACKNOWLEDGMENTS
The supportive assistance of rehabilitation staff at Kawamura Hospital
during planning of the experiment is gratefully acknowledged.
GRANTS
This work was partly supported by Grant-in-Aid for Young Scientists (B)
25750203 (to I. Nojima) from the Japan Society for the Promotion of Science.
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the author(s).
AUTHOR CONTRIBUTIONS
Author contributions: T.W. and I.N. conception and design of research;
T.W., S.K., and S.T. performed experiments; T.W. analyzed data; T.W. and
I.N. interpreted results of experiments; T.W. prepared figures; T.W. drafted
manuscript; T.W. and I.N. edited and revised manuscript; T.W. and I.N.
approved final version of manuscript.
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under spatial incompatibility, and their facilitation effects on
RTs did not remain until foot lift in the Simon task.
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