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Lasting Effects of Adaptive Visual Reweighting on Postural Control in Young Adults

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Postural control involves the use of sensory cues that must be properly integrated to provide specific information to accommodate continuous changes in the environment. Studies have shown several features of adaptive sensorimotor behavior, but many of the mechanisms are still unknown, such as perdurable effects. The purpose of the present study was to examine the lasting effects of visual reweighting adaptation on postural control in young adults. Seventeen young adults were exposed to a moving room situation in 3 experimental sessions that occurred on different occasions. In the first occasion, participants were exposed to seven 60-s trials, in which the room oscillated sinusoidally (0.2 Hz). The first 3 trials and last 3 trials had an amplitude of 0.6 cm and velocity of 0.6 cm/s (peak-to-peak). The fourth trial had an amplitude of 3.5 cm and velocity of 3.5 cm/s (change trial). In the second and third occasions, 1 and 7 days after the first occasion, respectively, the participants performed 3 trials with the room moving with the same parameters as the first trial in the first occasion. The results indicated that the abrupt increases in amplitude and velocity led to a less coherent and smaller magnitude of postural response to the moving room. The reduction of the induced postural response that was caused by visual manipulation lasted at least 1 week. These results suggest that adaptive changes that are caused by environmental changes are maintained for a relatively long period of time in young adults.
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Lasting Effects of Adaptive Visual Reweighting on Postural Control
in Young Adults
Giovanna Gracioli Genoves
Universidade Estadual Paulista
Ana Maria Forti Barela
and Stefane Aline Aguiar
Universidade Cruzeiro do Sul
José Angelo Barela
Universidade Estadual Paulista and Universidade Cruzeiro do Sul
Postural control involves the use of sensory cues that must be properly integrated to
provide specific information to accommodate continuous changes in the environment.
Studies have shown several features of adaptive sensorimotor behavior, but many of the
mechanisms are still unknown, such as perdurable effects. The purpose of the present
study was to examine the lasting effects of visual reweighting adaptation on postural
control in young adults. Seventeen young adults were exposed to a moving room
situation in 3 experimental sessions that occurred on different occasions. In the first
occasion, participants were exposed to seven 60-s trials, in which the room oscillated
sinusoidally (0.2 Hz). The first 3 trials and last 3 trials had an amplitude of 0.6 cm and
velocity of 0.6 cm/s (peak-to-peak). The fourth trial had an amplitude of 3.5 cm and
velocity of 3.5 cm/s (change trial). In the second and third occasions, 1 and 7 days after
the first occasion, respectively, the participants performed 3 trials with the room
moving with the same parameters as the first trial in the first occasion. The results
indicated that the abrupt increases in amplitude and velocity led to a less coherent and
smaller magnitude of postural response to the moving room. The reduction of the
induced postural response that was caused by visual manipulation lasted at least 1
week. These results suggest that adaptive changes that are caused by environmental
changes are maintained for a relatively long period of time in young adults.
Keywords: posture, sensorimotor adaptation, moving room, reweighting, visual manip-
ulation
Adaptation has long been acknowledged as
an important aspect of the postural control sys-
tem that provides flexibility and functionality
(i.e., Forssberg & Nashner, 1982). Based on
changes in sensory cues (i.e., changes in the
environment), the central nervous system mod-
ulates postural responses in adults (Barela et al.,
2014;Dijkstra, Schöner, & Gielen, 1994;Jeka,
Oie, Schöner, Dijkstra, & Henson, 1998;Oie,
Carver, Kiemel, Barela, & Jeka, 2005;Oie, Ki-
emel, & Jeka, 2002;Schöner, Dijkstra, & Jeka,
1998), typically developing children (Rinaldi,
Polastri, & Barela, 2009), special needs children
(Barela et al., 2011), and older adults (Barela,
Genoves, Alleoni, & Barela, 2013). Such a pro-
cess has been referred to as sensory reweight-
ing, in which the postural control system adap-
tively down-weights or up-weights the sensory
influence using sensory inputs that provide the
most precise and useful information to optimize
stance control. Adaptive mechanisms are needed
and extremely important to determine the way in
This article was published Online First May 22, 2017.
Giovanna Gracioli Genoves, Laboratório para Estudos do
Movimento, Departamento de Educação Física, Instituto de
Biociências, Universidade Estadual Paulista; Ana Maria
Forti Barela and Stefane Aline Aguiar, Instituto de Ciências
da Atividade Física e Esporte, Universidade Cruzeiro do
Sul; José Angelo Barela, Laboratório para Estudos do Mo-
vimento, Departamento de Educação Física, Instituto de
Biociências, Universidade Estadual Paulista, and Instituto
de Ciências da Atividade Física e Esporte, Universidade
Cruzeiro do Sul.
Correspondence concerning this article should be ad-
dressed to José Angelo Barela, Departamento de Educação
Física, Instituto de Biociências, Universidade Estadual
Paulista, Campus Rio Claro, Rua 24-A, 1515, São Paulo,
SP, 15506-900, Brazil. E-mail: jbarela@rc.unesp.br
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This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Psychology & Neuroscience © 2017 American Psychological Association
2017, Vol. 10, No. 2, 243–251 1983-3288/17/$12.00 http://dx.doi.org/10.1037/pne0000086
243
which and under which circumstances multiple
sensory modalities are weighted, thus modifying
the influence of specific sensory cues on postural
responses.
To examine sensory reweighting, sensory
stimulus amplitude and velocity have been ma-
nipulated, and changes in postural responses
have been observed (Barela et al., 2014;Oie et
al., 2005) and even mathematically modeled
(Carver, Kiemel, & Jeka, 2006;Carver, Kiemel,
van der Kooij, & Jeka, 2005;Schöner et al.,
1998). The results from these studies have in-
dicated that the coupling between sensory infor-
mation and body sway is stronger at a low
amplitude of driving signals, and such coupling
decreases as the stimulus amplitude is increased
within a single modality (i.e., intramodality;
Barela et al., 2014;Jeka, Oie, & Kiemel, 2008)
and across different sensory modalities (i.e.,
intermodality; Polastri, Barela, Kiemel, & Jeka,
2012). These findings suggest that the function
of the postural control system is a nonlinear
process (Carver et al., 2005;van der Kooij,
Jacobs, Koopman, & van der Helm, 2001). In
both cases, an abrupt increase in magnitude of
the sensory cue leads to a dramatic drop in the
observed postural response that is caused by
sensory manipulation. The effects of sensory
reweighting on postural responses have also
been observed by manipulating two conflicting
sensory modalities simultaneously (Barela,
Bonfim, & Polastri, 2006;Polastri et al., 2012;
Razuk, Viana, & Barela, 2013).
In addition to evidence that indicates that
body sway depends on the magnitude of sensory
stimuli, recent studies (Jeka et al., 2008;Polastri
et al., 2012) have also shown that the postural
control system has different adaptive mecha-
nisms in the reweighting process. For example,
abruptly increasing the visual stimulus ampli-
tude led to a rapid drop in gain of the visual
stimulus, whereas abruptly decreasing the vi-
sual stimulus amplitude led to a much slower
increase in gain (Jeka et al., 2008;Barela, To-
ledo, Ferreira, & Polastri, 2009), suggesting
temporal asymmetry in the adaptation of the
postural response to changes in the surrounding
visual environment (Jeka et al., 2008). Polastri
et al. (2012) also observed abrupt changes
within a short period of time and small changes
that occurred over a longer period of time, in-
dicating fast and slow adaptive mechanisms,
respectively, of the postural control system.
These results are consistent with the adaptive
postural model of Carver et al. (2006), which
suggests a functional role of temporal asymme-
try. The system can quickly decrease the re-
sponse to a sensory stimulus that might lead to
large deviations of the upright stance or even a
risk of falling. Slower responses to sensory
stimuli are observed when such stimuli do not
threaten postural equilibrium. Observations of
both mechanisms demonstrate the complexity
and adroitness of the postural control system,
such that its functioning prevents both danger-
ous destabilization and changes that might lead
to unnecessary energy expenditure (Carver et
al., 2005). Therefore, flexible and adaptive be-
havior of the postural control system entails
both magnitude and time scale adjustments to
modulate postural responses.
Despite the recently acquired knowledge
about the reweighting process that has eluci-
dated the mechanisms of postural control by
measuring responses to single or multiple sen-
sory modalities, still unknown is the longevity
of these postural responses that are caused by
reweighting. The experimental procedures of
these studies usually exposed participants to
different stimulus amplitudes that lasted from 1
min (Barela et al., 2011;Barela et al., 2013;
Barela et al., 2014) to several minutes (Aguiar
& Barela, 2015;Jeka et al., 2008;Polastri et al.,
2012;Rinaldi et al., 2009), and adaptive behav-
ior was observed within these short periods of
time. However, what is unclear is how long
such adaptive effects endure. Long-term adap-
tive changes are important for determining
whether the central nervous system takes advan-
tage of prior experience to shape and tune sub-
sequent responses over a longer period of time.
Therefore, the purpose of the present study was
to examine the long-term effects of visual re-
weighting adaptation on postural control in
young adults.
Method
Participants
Seventeen healthy young adults participated
as volunteers in this study (20.9 3.5 years old;
72.5 11.8 kg body mass, 171.8 8.0 cm
height). All of the participants were undergrad-
uate students, had normal or corrected-to-
normal vision, and reported no musculoskeletal
244 GENOVES, BARELA, AGUIAR, AND BARELA
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disorder that could interfere with their balance.
All of the volunteers agreed to participate in the
study and provided written informed consent.
The procedures were approved by the institu-
tional review board.
Apparatus and Procedures
The participants were exposed to three exper-
imental sessions that occurred on different oc-
casions. In each occasion, their task was to
remain upright inside a moving room in 60-s
trials. They were instructed to remain as still as
possible while looking straight ahead toward a
target that was placed 1 m away on the front
wall at eye level.
The dimensions of the moving room were
2.1 m (length) 2.1 m (width) 2.1 m
(height). The room consisted of three walls and
a ceiling that were positioned on wheels that
allowed movement in the anterior-posterior di-
rection (i.e., back and forth), independent of the
floor, which remained stationary the entire time.
The room movement was produced by a servo-
motor mechanism (Ottime, model SM23
SSF1192108, Compumotor, CA, USA) and
controlled by Motion Planner 4.3 software. The
inside walls of the room were painted white
with black stripes, creating a pattern of 42 cm
wide vertical white stripes and 22 cm wide
vertical black stripes. The target on which the
participants were instructed to fixate wasa5cm
diameter white circle that was positioned on a
black stripe attached to the center of the front
wall. A 20-W lamp that was attached to the
ceiling of the room provided consistent illumi-
nation throughout data collection.
At the beginning of the experiment, the par-
ticipants were unaware about the movement of
the room. To ensure their lack of knowledge
regarding this movement, white noise was used
to mask possible sounds that emanated from the
motor that generated the room movement. The
wheels on which the room was moved and
the motor were also visually covered so the
participants could not see them.
In the first occasion that the participants vis-
ited the laboratory (experimental Session 1),
data from seven 60-s trials were acquired. In the
first three trials (prechange trials), the room was
moved with a 0.2 Hz frequency, 0.6 cm/s peak-
to-peak velocity, and 0.6 cm amplitude. In the
fourth trial (abrupt-change trial), the room was
moved at a 0.2 Hz frequency, 3.5 cm/s peak-to-
peak velocity, and 3.5 cm amplitude. In the last
three trials (postchange trials), the room was
moved with the same parameters as the first
three trials (i.e., 0.2 Hz frequency, 0.6 cm/s
peak-to-peak velocity, and 0.6 cm amplitude).
The parameters that were adopted for the pre-
and postchange trials were based on previous
studies, in which the participants were unable to
perceive that the room was moving but were
still influenced by the movement and presented
corresponding body sway (Barela et al., 2014;
Freitas Júnior & Barela, 2004). The parameters
for the abrupt-change trial were based on a
previous study, in which the movement induced
adaptive responses in young adults (Barela et
al., 2014).
Experimental Session 2 occurred 24 hr af-
ter experimental Session 1. In this occasion,
the participants returned to the laboratory the
next day and performed three trials (post-1-
day trials) in which the room movement pa-
rameters were the same as in the prechange
and postchange trials that were performed in
the first occasion (0.2 Hz frequency, 0.6 cm/s
peak-to-peak velocity, and 0.6 cm amplitude).
Experimental Session 3 occurred 1 week
after experimental Session 1 and consisted of
three trials (post-1-week trials) that were
identical to those performed in experimental
Session 2. The participants were not informed
about the room movement in any of the ex-
perimental sessions, although the majority of
them reported that the room had moved after
the abrupt-change trial. When such a report
occurred, the experimenters neither confirmed
nor denied the movement of the room and
only instructed the participants to remain as
still as possible. In the following trials, both
on the same day and on subsequent days, none
of the participants reported any movement of
the room.
Body sway and moving room displacement
data were acquired using the OPTOTRAK 3020
3D Motion Measurement System (Northern Dig-
ital Inc., ON, CA) and infrared markers that were
placed on the participants’ back (at the level of the
eighth thoracic vertebra) and on front wall of the
room. The data were acquired at a frequency of
100 Hz in the anterior-posterior, medial-lateral,
and vertical directions.
245ADAPTIVE VISUAL REWEIGHTING IN POSTURAL CONTROL
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Data Analysis
Considering that the manipulations of room
movement occurred only in the anterior-
posterior direction, all of the analyses of body
sway, room movement, and body sway cou-
pling were performed only for this direction.
The dependent variables were mean sway am-
plitude, coherence, and gain.
The mean sway amplitude was used to indi-
cate overall sway magnitude, even though sway
occurred at frequencies other than the one that
was induced by the moving room. The mean
sway amplitude was calculated as the standard
deviation of the participants’ trunk position. Be-
fore obtaining the standard deviation, the aver-
age trunk position and a first-order polynomial
were subtracted from the trunk position time
series to avoid the possible influence of changes
in postural orientation that were unrelated to
maintaining an upright stance.
To analyze relationships between room
movement and body sway, coherence and gain
were used. Coherence was computed as the
square of the cross-spectrum between the two
signals (room movement and body sway), di-
vided by the autocorrelation of the Fourier
transforms of the room movement signal mul-
tiplied by the autocorrelation of the Fourier
transforms of the body sway signal, which was
calculated only at the driving stimulus fre-
quency (i.e., 0.2 Hz). Coherence indicated the
strength of the relationship between body sway
and room movement. Coherence values close to
1 indicated strong dependence between the two
signals, and values close to 0 indicated weak or
no dependence between the signals.
To calculate gain, a frequency response func-
tion was derived from the trunk sway Fourier
transforms divided by the visual stimulus Fou-
rier transforms. Gain was the absolute value of
the transfer function calculated at the driving
frequency (i.e., 0.2 Hz). Gain values indicated
the magnitude of the influence of room move-
ment on body sway. Gain values 1 indicated
that the spectrum of body sway was greater than
the spectrum of the room movement signal at
the driving frequency, and values close to 0
indicated that the spectrum of body sway was
lower than the spectrum of room movement at
this frequency.
Statistical Analysis
Comparisons among the different experimental
conditions were conducted using repeated-
measures analyses of variance (ANOVAs), with
condition (prechange, abrupt-change, postchange,
post-1-day, and post-1-week) as the main factor
for each dependent variable. For all variables, the
average from the three trials for each condition
(prechange, postchange, post-1-day, and post-1-
week; not including abrupt-change) was used for
the statistical analysis. When necessary, the Tukey
honestly significant difference post hoc test was
used. Planned comparisons were used to compare
the prechange and abrupt-change conditions, pre-
change and postchange conditions, prechange and
both post-1-day and post-1-week conditions to-
gether, postchange and both post-1-day and post-
1-week conditions together, and post-1-day and
post-1-week conditions. The level was 0.05 for
all of the analyses.
Results
Visual manipulation induced coherent pos-
tural sway in the prechange trials (i.e., before
the visual stimulus magnitude increased). When
the visual stimulus magnitude was increased,
induced postural sway dramatically decreased
and remained lower even after the 1-week pe-
riod. Figure 1 shows exemplar time series of
moving room displacement and body sway be-
fore the visual stimulus magnitude increased
(Figure 1a), in the trial in which the visual
stimulus magnitude increased (Figure 1b), and
after 1 week (Figure 1c).
Figure 2 shows the mean values of mean
sway amplitude across all conditions. The
ANOVA revealed a significant effect of condi-
tion (F
4,64
7.01, p.001). The mean sway
amplitude was greater in the abrupt-change con-
dition than in the prechange condition (p
.005).
Figure 3 shows the mean coherence values
across all conditions. The ANOVA revealed a
significant effect of condition (F
4,64
10.65,
p.001). Coherence was greater in the pre-
change condition than in the abrupt-change con-
dition (p.001). Coherence was also greater in
the prechange condition than in both the post-
1-day and post-1-week conditions (p.005).
Figure 4 shows the mean gain values across
all conditions. The ANOVA revealed a signifi-
246 GENOVES, BARELA, AGUIAR, AND BARELA
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This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
cant effect of condition (F
4,64
33.43, p
.001). Gain was higher in the prechange condi-
tion than in the abrupt-change (p.001) and
postchange (p.005) conditions. Gain was
also higher in the prechange condition than in
both the post-1-day and post-1-week conditions
(p.001).
Discussion
The purpose of the present study was to ex-
amine the lasting effects of visual reweighting
adaptation on postural control in young adults.
The results showed that participants were influ-
enced by the visual manipulation, reflected by
Figure 1. Exemplar time series of trunk sway (OCap) and moving room displacement
(SMap) in the (a) prechange, (b) abrupt-change, and (c) post-1-week conditions.
Figure 2. Mean sway amplitude values (mean and standard deviation) across all five trial
conditions.
p.05, significant difference between conditions.
247ADAPTIVE VISUAL REWEIGHTING IN POSTURAL CONTROL
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coherent oscillation with the movement of the
room. An increase in the visual stimulus mag-
nitude led to reweighting the influence of the
visual stimulus on postural sway, and such re-
weighting was still evident during the subse-
quent visual exposures (immediately afterward,
1 day later, and 7 days later). Therefore, adap-
tive changes that were caused by an increase in
the visual magnitude lasted for up to 1 week.
The observation that visual manipulation in-
duces corresponding and coherent postural
sway has been extensively documented (Barela,
Barela, Rinaldi, & de Toledo, 2009;Barela,
Toledo, et al., 2009;Barela et al., 2014;Freitas
Figure 3. Mean (standard deviation) coherence values across all five trial conditions.
p.05,
significant difference between conditions.
Figure 4. Mean (standard deviation) gain values across all five trial conditions.
p.05,
significant difference between conditions.
248 GENOVES, BARELA, AGUIAR, AND BARELA
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Júnior & Barela, 2004). Despite the lack of
novelty of the present study (i.e., our results
corroborate previous studies), we found that
small-amplitude and low-velocity visual manip-
ulations were sufficient to induce postural sway
while the participants were unaware that sen-
sory manipulations were occurring. Such body
sway was highly correlated with the sensory
manipulation (coherence and gain 1), indi-
cating that intrinsic dynamics indeed are em-
bedded in the postural control system (Aguiar &
Barela, 2014). Such dynamics are quite impor-
tant for the proper functioning of the postural
control system because they free the system to
perform other activities and engage mecha-
nisms other than those that are required to com-
pare and respond to small changes in sensory-
motor coupling.
Despite showing unconscious, dynamic cou-
pling to small sensory manipulations, when
changes in the sensory stimulus exceed a certain
amplitude/velocity, the postural control system
is able to uncouple from the sensory stimulus.
This was the case when the visual stimulus
amplitude/velocity was increased in the abrupt-
change trial. Instead of coupling to the visual
stimulus as had previously happened, the pos-
tural control system down-weighted the influ-
ence of the visual stimulus, showing signifi-
cantly lower gain and coherence values and
indicating a much lower influence of the visual
stimulus, consistent with previous studies
(Barela et al., 2014;Jeka et al., 2008). Notably,
this does not mean that body sway did not
occur. Actually, the magnitude of body sway
increased (see Figure 2), but such oscillations
were much less related to the visual manipula-
tion and most likely occurred as a consequence
of the attempt of the postural control system to
avoid visual influences. The sharp drop in gain
that was caused by an abrupt increase in stim-
ulus amplitude is a signature aspect of the pos-
tural control system because it can prevent pos-
sibly large undesirable effects of a threatening
sensory stimulus (Carver et al., 2006;Jeka et al.,
2008). If the postural control system exhibits
the same coupling strength and high gain in
response to a large stimulus amplitude, then the
system could be “knocked out” and the upright
stance orientation could be compromised. Such
a drop in gain might have occurred because of
the awareness of room movement by the partic-
ipants in the abrupt-change trial. Interestingly,
however, after the abrupt increase in the visual
amplitude and velocity, participants who were
consciously and unconsciously aware of room
movement showed similar reductions of the
coupling of visual stimulus and body sway
(Barela et al., 2014). Therefore, flexible and
continuous adjustments of sensory influences
on postural control (i.e., down-weighting and
up-weighting the influence of sensory stimuli)
are important for the efficiency and functional-
ity of such a complex system.
The present results advance our understand-
ing of the adaptive mechanisms of the postural
control system. When the system was exposed
to a situation in which the sensory weight was
altered, such changes were maintained for at
least 1 week. The gain and coherence values
were lower than those observed in the abrupt-
change trial, even 1 week after exposure. Such
a result is remarkable because it shows that the
postural control system is able to down-weight
the influence of the visual stimulus in response
to a change in amplitude, which provides sev-
eral functional advantages when employing one
(Barela et al., 2014;Jeka et al., 2008) and two
(Polastri et al., 2012) sensory modalities. The
postural control system is able to maintain such
adaptation for a relatively long period of time.
Therefore, the prolonged effect of adaptive
change constitutes another functional postural
control mechanism, in which the system does
not need to switch back to its original state, thus
preserving the down-weighting that was previ-
ously acquired. If the postural control system
reverts back to the prechange weighting of the
influence of the stimulus, then it would have to
undergo the same adaptive change in the case of
exposure to the same change in the sensory
condition. Altogether, these results indicate that
down-weighting a sensory modality in response
to changes in environmental motion has both
positive and negative effects on postural control
(Polastri et al., 2012). The postural control sys-
tem adopts a strategy to carry over the change in
sensory motor coupling. By preserving the
change, the system likely optimizes its function
because it does not have to keep switching to
different functional states.
Carver et al. (2006) suggested that down-
weighting the influence of a sensory stimulus
(e.g., vision) on postural sway over a few sec-
onds does not greatly threaten upright stability
under normal environmental conditions because
249ADAPTIVE VISUAL REWEIGHTING IN POSTURAL CONTROL
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the postural control system can still accomplish
the goal of standing upright. These authors sug-
gested that such a strategy optimizes metabolic
energy expenditure. Our results showed that if
this was true, then young adults take advantage
of lower metabolic energy expenditure over a
much longer period of time (i.e., days). Al-
though sensory reweighting is considered criti-
cal for postural control, little attention has being
given to possible asymptotic responses to sen-
sory reweighting that is induced by long trials
(Carver et al., 2006). The present study evalu-
ated the asymptotic response over a relatively
long period of time, indicating that the central
nervous system fully adapts and equilibrates in
response to the new visual stimulus with less
responsive sway, even over days. Considering
the functional advantage of such behavior, the
central nervous system takes advantage of prior
exposure to a different visual stimulus, even
days after such exposure. Unresolved issues in-
clude how long such an adaptive change can be
preserved, how it returns to its original state,
and whether it can return to its original state.
Other important issues are related to the speci-
ficity of these adaptive behavioral changes,
whether adaptive changes that are observed in a
specific condition or environment are transfer-
able to other conditions or novel environments,
and whether similar adaptive changes occur in
other sensory modalities. These issues should
be addressed in future studies.
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Received May 24, 2016
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Accepted April 20, 2017
251ADAPTIVE VISUAL REWEIGHTING IN POSTURAL CONTROL
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