Neuroscience 234 (2013) 2230

ELDERLY ADULTS DELAY PROPRIOCEPTIVE REWEIGHTING DURING

THE ANTICIPATION OF COLLISION AVOIDANCE WHEN STANDING
D. J. A. EIKEMA, a V. HATZITAKI, a*
V. KONSTANTAKOS b AND C. PAPAXANTHIS c,d

seems to be a more time consuming process in aging which

may have important clinical implications for falling.
2013 IBRO. Published by Elsevier Ltd. All rights reserved.

Motor Control and Learning Laboratory, Department of

Physical Education and Sport Science, Aristotle University of
Thessaloniki, Hellas, Greece

Key words: balance, falls, aging, vision, proprioception, sensory reweighting.

Electronics Laboratory, Physics Department, Aristotle University

of Thessaloniki, Hellas, Greece

Universite de Bourgogne, Unite de Formation et de Recherche

en Sciences et Techniques des Activites Physiques et Sportives,
F-21078 Dijon, France

INTRODUCTION

Institut National de la Sante et de la Recherche Medicale

(INSERM), 1093, Cognition, Action, and Plasticite Sensorimotrice,
BP 27877, F-21078 Dijon, France

During closed loop control of posture, vision, lower limb

proprioception and vestibular sensation each provide
information on a unique aspect of the environment and
ones orientation in it (Peterka, 2002). The contribution
of the sensory modalities to the internal representation
of the environment varies depending on the weight the
CNS assigns to each modality. As environmental
conditions change, the weight assigned to a particular
modality may need to be adjusted (i.e. reweighted)
depending on its estimated accuracy for the control of
posture (Peterka and Loughlin, 2004). For example, the
accuracy of proprioceptive input is reduced when
standing on a sway- and reverse-sway-referenced
support surface (Doumas and Krampe, 2010) or during
bilateral application of Achilles tendon vibration (Eklund,
1972). Similarly, the accuracy of visual input is reduced
by optic ow manipulations (OConnor et al., 2008) or
changes in visual stimuli motion (Jeka et al., 2006), both
requiring the down-weighting of visual input. The
transition from one weighting conguration to another
leads to a temporary imbalance of weights which results
in increased postural instability (Peterka and Loughlin,
2004). Through eective sensory reweighting, this
instability is progressively reduced as a function of
adaptation (Jeka et al., 2008).
In older adults, ambiguous environments requiring the
reweighting of sensory inputs could increase the risk of
falling (Hay et al., 1996; Teasdale and Simoneau,
2001). This is because normal aging delays the process
of sensory reweighting resulting in prolonged postural
instability when proprioceptive (Doumas and Krampe,
2010) and/or visual input is altered (Jeka et al., 2010).
Particularly, both healthy and fall-prone older adults
show a more persistent increase in postural sway when
they are exposed to changes in optic ow (OConnor
et al., 2008) or visual motion stimulation (Jeka et al.,
2010). An insucient and delayed down-weighting of
the inaccurate visual cues could be due to increased
visual eld dependence (Isableu et al., 1998). Visual
eld dependence is a measure of the reliance on visual

AbstractThe ability to reweight visual and proprioceptive

information is critical for maintaining postural stability in a
dynamic environment. In this study, we examined whether
visual anticipation of collision avoidance (AV) while standing could facilitate the down-weighting of altered proprioception in young and elderly adults. Twelve young
(24.91 6.44 years) and 12 elderly (74.8 6.42 years) participants stood upright for 180 s under two task conditions:
(a) quiet stance (QS) and (b) standing while anticipating virtual objects to be avoided. In order to disrupt the accuracy
of proprioceptive input participants were exposed to bilateral Achilles tendon vibration during the middle 60 s of
standing in both tasks. Visual eld dependence was
assessed using the Rod and Frame Test (RFT). Elderly demonstrated signicantly higher visual eld dependence compared to the young participants. Analysis of the normalized
Root Mean Square (RMS) of the Center of Pressure velocity
(dCoP) revealed that young participants immediately
reduced the sway velocity variability induced by tendon
vibration during the anticipation of collision AV compared
to the QS task. In the elderly, however, the modulating inuence of visual anticipation was delayed and became signicant only in the last two time intervals of the vibration
phase. These results suggest that volitionally shifting reliance on vision when anticipating a collision AV event facilitates the down-weighting of altered proprioception.
Elderly adults seem to be unable to dynamically exploit
visual anticipation in order to down weight the altered proprioception possibly as a result of their more permanent
up-weighting of the visual modality. Sensory reweighting

*Corresponding author. Tel/fax: +30-2310-992193.

E-mail address: vaso1@phed.auth.gr (V. Hatzitaki).
Abbreviations: ANOVA, analysis of variance; AV, avoidance; C7, 7th
cervical vertebra; dCoP, Center of Pressure velocity; ML, Medio
Lateral; MMSE, Mini Mental Status Examination; QS, quiet stance;
RFT, Rod and Frame Test; RMS, Root Mean Square; ST, stabilization
time; T1T5, time intervals 1 to 5.

0306-4522/12 $36.00 2013 IBRO. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.neuroscience.2012.12.053
22

D. J. A. Eikema et al. / Neuroscience 234 (2013) 2230

cues for the perception of verticality (Reger et al., 2003).

Increased visual eld dependence suggests that older
adults rely more on visual input for postural corrections,
even when visual accuracy is compromised (Sundermier
et al., 1996; Simoneau et al., 1999). As a result, they
are unable to centrally suppress the unreliable visual
cues in the presence of visual motion perturbations
(OConnor et al., 2008; Jeka et al., 2010). The ability to
centrally suppress the inaccurate sensory input, called
perceptual inhibition, correlates with the ability to shift
attention between sensory modalities during balancechallenging tasks (Redfern et al., 2001, 2009). Thus, an
age-induced overreliance on visual information may be
disruptive for postural control due to the delayed down
weighting of the inaccurate visual cues.
We have recently examined how the visual anticipation
of randomly approaching objects to be avoided (i.e.
collision avoidance (AV) modulates the process of visual
reweighting in young and healthy elderly adults (Eikema
et al., 2012). Down-weighting of visual input was evoked
by either removal or periodic motion of the visual
surround. Visual anticipation under conditions of visual
ambiguity imposes an intra-sensory conict. On one
hand, the ambiguous visual environment requires the
down-weighting of vision in order to maintain a stable
posture. On the other, visual information needs to remain
of high priority to successfully detect and avoid the
randomly approaching objects. In quiet standing, visual
reweighting was impaired only in older adults due to their
greater visual eld dependence. Visual anticipation
impaired visual reweighting, i.e. increased sway in
response to the visual perturbation, independently of age.
This is because the anticipation of the visual, possibly
balance-threatening events modulated the reweighting
process by increasing the anchoring to vision (Ohno
et al., 2004; Ishida et al., 2010). What is still not known
however is whether the increased anchoring to vision
evoked by anticipation of collision avoidance can
modulate the down-weighting of a non-visual modality
such as proprioception when its accuracy is
compromised. In a recent study, Isableu et al. (2011)
have shown that increasing proprioceptive reliance by
active forward or backward body leaning helped
participants to reduce or suppress the destabilizing
eects of altered vision on body posture. Nevertheless,
large inter-individual dierences in beneting from the
increased proprioceptive reliance were noted.
In the current study, we investigated whether
increasing volitional reliance on vision through the
anticipation of collision avoidance events could facilitate
the down-weighting of altered proprioceptive input in
both young and elderly adults. Proprioception was
perturbed by the bilateral application of Achilles tendon
vibration during the middle 60 s of a 180-s stance trial.
Vibration alters proprioceptive input of the triceps surae
muscles resulting in a posterior postural shift during
standing (Eklund, 1972). Specically, we predicted that
sway velocity variability evoked by Achilles tendon
vibration would be reduced during anticipation compared
to quiet standing in both age groups. Because normal
aging slows the process of sensory reweighting we

23

expected a greater facilitation of the proprioceptive

reweighting due to visual anticipation in young
compared to elderly adults.

EXPERIMENTAL PROCEDURES
Participants
Twelve young (ve males, seven females; age 24.91 6.44,
mass 70.91 kg 13.93) and 12 elderly (six males, six females;
age 74.8 6.42, mass 78.44 kg 13.16) adults participated in
the study. Participants were free of neurological and
musculoskeletal impairments and had normal or corrected to
normal vision. The elderly participants performed the Mini
Mental Status Examination (MMSE) in order to ensure they
possessed the cognitive capacity to understand the instructions
and perform the tasks. The MMSE cut-o score was set at 22.
In the current study all elderly participants scored in the 2630
range of the MMSE. Participants were informed of the
procedures and provided written consent. All experiments were
performed with the approval of the local ethics committee on
human research in accordance with the Declaration of Helsinki.

Apparatus
Postural sway was recorded using a 3-D force plate (Balance
Plate 6501, Bertec Corporation, Columbus, USA) at a sampling
rate of 105 Hz. Kinematics were captured using an
electromagnetic tracking system (Nest of Birds, Ascension Inc.,
Burlington, USA). A single marker was placed on the 7th
cervical vertebra (C7). The virtual visual surround and visual
stimuli were delivered by a stereoscopic projection screen
(Barco Baron 908, Barco N.V., Kuurne, Belgium, width 128 cm,
height 102 cm) viewed through active shutter goggles (Crystal
Eyes 3, Stereographics) at 55 Hz per shutter. The screen was
located 200 cm from the participant providing a horizontal
viewing angle of 38. The virtual environment consisted of an
empty room with walls, oor, and ceiling textured with an
alternating light and dark grey bar pattern (Fig. 1a).
Proprioception was altered using bilateral Achilles tendon
vibration using a pair of tendon vibrators (VB115,
Technoconcept, France).

Task and procedure

The participants performed the Rod and Frame Test (RFT) in
order to determine the degree of visual eld dependence
(Reger et al., 2003), indicating the degree to which an
individual relies on visual information for postural corrections
(Isableu et al., 1998). During the task, a rod was visible inside
a frame, which would be tilted +18, 0 or 18. Using a handheld marker of the electromagnetic tracking system, the
participant was repeatedly asked to rotate the bar while
standing until it was estimated to be vertical. The angular
deviation of the rods nal position from the actual vertical was
recorded as error in degrees.
Prior to the experimental trials, participants were familiarized
with the visual collision AV task. The visual target stimulus was a
sphere (10 cm in diameter, textured to resemble a green tennis
ball) traveling at a constant velocity from the center of the
visual eld towards the participants head (Fig. 1a). Participants
were instructed to avoid collision with the sphere by displacing
their trunk and head together as a unit along the MedioLateral
(ML) axis, without moving the feet. Head-centered collision AV
movements (increased head movements while displaying
minimal trunk displacement) were discouraged as this could
compromise postural stability. Particularly, moving the head

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D. J. A. Eikema et al. / Neuroscience 234 (2013) 2230

Fig. 1. (a) An illustration of the visual surround (i.e. virtual room) during the quiet stance (QS) task and target stimuli (i.e. virtual sphere) presented in
the collision avoidance (AV) task. The virtual room consisted of an alternating light and dark grey bar pattern to optimally stimulate the visual system.
(b) Representative Center of Pressure (CoP) time series in the MedioLateral (ML) direction during a single 12 s interval of the collision AV task.
During each 12-s interval, a spherical object was quasi-randomly presented between 4 and 8 s, on an intersect course with the participant. The 4-s
stance period prior to the appearance of the object on the screen was selected to calculate the Root Mean Square (RMS) of the CoP velocity.
Collision AV was followed by stabilization time (ST), during which the participant regained postural stability. (c) Representative Center of Pressure
(CoP) time series in the ML direction during the AV task. This shows the breakdown of the time intervals (T1T5) and the occurrence of AV
movements for each of the three 60-s phases of the QS and AV tasks.

with respect to the trunk during the AV might increase vestibular

input to the control of balance (Di Fabio and Emasithi, 1997). The
AV was successful if the target spheres end-coordinates were
outside a circular 20-cm range around the C7 marker
coordinates. During the familiarization trial, the participant
received feedback on successful AV. After each AV response,
the participant returned to the initial position. Anticipatory
leaning in the ML direction was controlled by providing visual
feedback when anticipatory leaning was detected. The velocity
of the target object was initially set at 200 cm/s and then was

gradually reduced until a 90% successful AV rate (nine out of

10 successful AVs within a single trial) was achieved. Target
velocity was individually adjusted to the participants AV
capacity in the familiarization phase and was held constant in
the experimental collision AV trials. The average target velocity
was set at 148.54 cm/s 19.44 and 105.97 cm/s 11.24 for
the young and the old groups, respectively. The second part of
the familiarization phase consisted of exposure to Achilles
tendon vibration for 15 s in order to acquaint the participant
with the vibratory stimulus.

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D. J. A. Eikema et al. / Neuroscience 234 (2013) 2230

During the experiment participants stood on the force
platform in a relaxed position (eyes open, inter-malleolar
distance: 10 cm, arms freely hanging by the sides) and
performed two 180-s long postural tasks; a quiet stance (QS)
task and a collision AV task. In the AV task, 15 target stimuli
(i.e. virtual spheres) were delivered at quasi-random times,
each within a separate 12-s time interval. A restricted random
number generator selected a time in seconds between the 4th
and 8th s of the respective 12-s time window for the target
stimulus to be presented (Fig. 1b). During each task,
proprioceptive reweighting was evoked by bilateral Achilles
tendon vibration (3 mm, 80 Hz) during the middle 60 s. Thus,
each task consisted of three phases (Fig. 1c): (i) the initial 60 s
(pre-vibration phase) which served as the baseline in each trial
and provided accurate proprioceptive input, (ii) the middle 60 s
(vibration phase) and (iii) the nal 60 s (post-vibration phase)
where accurate proprioceptive input was re-inserted.

Data analysis
Center of Pressure (CoP) and trunk kinematic signals were
synchronously sampled at 105 Hz and further processed in
MatLab (Mathworks Inc., USA). Trunk kinematics yielded
similar results and as such they are not reported in this
manuscript. The CoP signal was low-pass ltered using a 4thorder zero-lag Butterworth lter with a 5-Hz cut-o frequency.
The CoP displacement was dierentiated to yield CoP velocity
(dCoP). The dCoP signal was segmented into ve 12-s time
intervals (T1T5) in order to quantify the adaptation within each
60 s phase of the task (Fig. 1c). For the QS task, CoP velocity
variability was quantied by calculating the Root Mean Square
(RMS) of the dCoP signal over the respective 12-s time
interval. For the AV task, RMS dCoP was calculated over a
time interval consisting of the 4 s before the collision AV event,
starting 4 s prior to object appearance and ending at object
appearance (indicated by a trigger pulse) (Fig. 1b). The object
was visible for a maximum duration of 2 s, depending on
the preset object velocity. A second pulse indicated when
the object was no longer visible. In order to ensure that the
participant returned to a stable postural equilibrium prior to the
4 s period that was used to calculate the RMS dCoP,
stabilization time (ST) was computed. ST was dened as the
time in seconds for which RMS dCoP pre-AV was greater than
RMS dCoP post-AV. ST was calculated using an AutoRegressive Moving Average model in which the expression (1 s
pre-AV RMS dCoP) P (1 s post-AV RMS dCoP) was
recursively evaluated. For the purpose of the present analysis,
we were only interested in the relative sway velocity variability
induced by vibration. We computed the normalized sway
velocity variability by dividing the RMS dCoP value at a given
time interval of the vibration and post-vibration phases by the
RMS dCoP of the corresponding time interval in the previbration (baseline) phase.

RESULTS
Visual eld dependence
Old group participants had signicantly higher RFT error
scores (F(1, 20) = 16.534, p < 0.001), suggesting they
were more visual eld dependent than the young
participants (Fig. 2). A signicant Group  Tilt interaction
was observed (F(2, 40) = 9.261, p < 0.001), indicating
that group dierences in error scores were dependent on
the tilting condition. Post hoc t-tests indicated that the
higher error scores observed in the Old group were only
signicant in the +18 and 18 tilting conditions. The
RFT error scores were not signicantly dierent between
groups in the 0 tilting condition.
Postural performance
Representative dCoP displacement time series of one
young and one older participant during the pre-vibration,
vibration and post-vibration phases of the QS task are
plotted in Fig. 3. It is evident that Achilles tendon
vibration increased sway velocity in both participants
although CoP velocity was greater for the old when
compared to the young participant. During the collision
AV trial, participants displayed a consistent preference
for rightward AV movements. Only three young and two
old participants demonstrated within-trial switching of AV
direction in more than ve out of 15 AV events.
Vibration phase. Normalized RMS dCoP values
(mean + standard deviation (SD)) for both groups and
tasks are plotted across the ve time intervals of the
vibration phase in Fig. 4. It appears that postural sway
velocity variability was concomitantly inuenced by the
motor task, the age group and the time interval. We found

Statistical analysis
Age dierences in visual eld dependence across the three tilting
directions were analyzed employing a 2 (Group)  3 (Tilt
direction) repeated measures analysis of variance (ANOVA) on
the RFT error scores. The normalized sway velocity variability
(RMS dCoP) was compared between tasks, groups and across
the time intervals by employing a 2 (Task: QSAV)  2 (Group:
YoungOld)  5 (Time interval: T1T5) repeated measures
ANOVA model that was performed separately for the vibration
and post-vibration phases. Signicant interaction eects were
further analyzed using post hoc paired samples t-tests between
the two tasks or between successive time intervals for each
group separately. Bonferroni adjustments were applied to
correct for multiple comparisons. p-Values were considered
signicant at p < 0.05.

Fig. 2. Mean error in the Rod and Frame Test (RFT) for the young
group (solid line) and the old group (dashed line), in each tilt
condition. Group means 1 standard error (SE) are shown.

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D. J. A. Eikema et al. / Neuroscience 234 (2013) 2230

Fig. 3. Representative Center of Pressure (dCoP) velocity (cm/s) time series in the Antero-Posterior (AP) direction of a young (black line) and an
older (grey line) participant during the pre-vibration, vibration and post-vibration phases of a the quiet stance (QS) trial. T1-T5 refers to the time
interval within each phase.

Fig. 4. Normalized Root Mean Square (RMS) of Center of Pressure velocity (RMS dCoP) for the young and old group across the ve time intervals
(T1T5) of the vibration phase. Group mean standard deviation (SD) values are plotted for the quiet stance (QS, dashed line, open circle) and the
avoidance (AV, solid line, lled circle) task. All values have been normalized with respect to the pre-vibration phase.

a main eect of Task on normalized RMS dCoP

(F(1, 22) = 12.63, p < 0.01) indicating that the relative
increase in sway velocity variability induced by Achilles
tendon vibration was signicantly greater in the QS
compared to the collision AV task. Interestingly, this
eect was not similar across age groups as conrmed
by a signicant Group  Task interaction eect
((F(1, 22) = 3.99, p < 0.05). Post hoc comparisons
between the two tasks indicated that the Young group
participants had signicantly lower normalized RMS
dCoP values in collision AV compared to QS in all ve

time intervals (p < 0.05) whereas for the Old group this
dierence was signicant only in the last two time
windows (T4: t(11) = 3.09, p < 0.01, T5: t(11) = 2.3,
p < 0.05; Fig. 4). Furthermore, a Time  Group
(F(4, 88) = 2.18, p < 0.05) and a Time  Task
(F(4, 88) = 2.49, p < 0.05) interaction suggest that the
vibration-induced variability decreased across successive
time intervals for the Old group in the AV task only
(Fig. 4). Specically, post hoc pair wise comparisons
across successive time intervals of the AV task conrmed
that the RMS dCoP signicantly increased between T1

D. J. A. Eikema et al. / Neuroscience 234 (2013) 2230

and T2 (t(11) = 1.8, p < 0.05) but decreased between T2

and T3 (t(11) = 2.32, p < 0.05) and between T3 and T4
(t(11) = 2.28, p < 0.05).
Post-vibration phase. Fig. 5 shows the normalized RMS
dCoP values (mean + SD) for the two groups and tasks
across the ve time intervals of the post-vibration phase. A
signicant Task  Group interaction on the normalized RMS
dCoP (F(1,22) = 4.94, p < 0.05) suggests that the eect of
the task was dependent on the age group. Indeed, post hoc
analysis indicated that for the Old group only, the vibrationinduced sway velocity variability was signicantly greater
during the AV than the QS task in the rst two intervals of
the post-vibration phase (T1: t(11) = 2.13, p < 0.05, T2:
t(11) = 1.98, p < 0.05). For the Young group on the other
hand, the normalized RMS dCoP was signicantly lower in
the AV than the QS task at intervals T1 and T5 (T1:
t(11) = 2.92, p < 0.05, T5: t(11) = 2.78, p < 0.05). A
highly signicant main eect of Time interval on the RMS
dCoP (F(4,88) = 45.36, p < 0.001) shows that this
decreased across successive time intervals. Nevertheless,
the rate of decrease was not the same across the two tasks
as this was conrmed by a signicant Time  Task
interaction eect (F(4, 88) = 3.73, p < 0.05). Further
post hoc analysis revealed that the adaptation was
slower during collision AV (signicant decrease between
T1T2, T2T3, p < 0.05 for both groups).
Furthermore, a signicant Time  Group interaction
(F(4, 88) = 3.19, p < 0.05) suggests that the adaptation
was slower for the Old compared to the Young group
participants.

DISCUSSION
The current study investigated the modulating inuence of
anticipating a collision avoidance event on the

27

reweighting of altered proprioception in young and

elderly adults. We focused on the degree of the evoked
proprioceptive disturbance (i.e. by tendon vibration) by
normalizing the sway velocity variability depicted during
the vibration and post-vibration phases to the variability
of the pre-vibration phase. The main nding of this
study is that anticipating collision avoidance events
immediately reduced the sway velocity variability evoked
by Achilles tendon vibration in young participants. In the
elderly however, the modulating inuence of visual
anticipation was delayed and became evident only as a
result of adaptation to the vibratory stimulus.
Visual anticipation of collision AV results in more
ecient proprioceptive reweighting
During quiet standing, Achilles tendon vibration resulted
in an almost 30% increase on sway velocity variability in
both age groups. Interestingly, when anticipating the
collision AV events, young participants immediately
reduced the sway velocity variability induced by tendon
vibration whereas elderly participants did not. Our
interpretation of this novel nding is that the anticipation
of collision AV events facilitated the transition from
proprioception to vision thereby resulting in a more
ecient
visual
up-weighting
and
subsequent
proprioceptive down-weighting. It is known that
anticipation of unpredictable aversive or balancethreatening events increases the anchoring to vision for
controlling balance (Ohno et al., 2004; Ishida et al.,
2010). Moreover, when proprioception is altered, either
by increasing the degree of postural leaning (Duarte and
Zatsiorsky, 2002; Isableu et al., 2011) or by standing on
a compliant surface (Anand et al., 2002), the reliance on
visual cues increases. This type of sensory transition
has been proposed as one possible driving mechanism

Fig. 5. Normalized Root Mean Square (RMS) of Center of Pressure velocity (RMS dCoP) for the young and old group across the ve time intervals
(T1T5) of the post-vibration phase. Group mean standard deviation (SD) values are plotted for the quiet stance (QS, dashed line, open circle)
and the avoidance (AV, solid line, lled circle) task. All values have been normalized with respect to the pre-vibration phase.

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D. J. A. Eikema et al. / Neuroscience 234 (2013) 2230

for the ecient reweighting of posture (Peterka and

Loughlin, 2004).
Age-associated visual eld dependence reveals a
delay in proprioceptive reweighting
Elderly participants could not immediately exploit the
anticipation of the collision AV events to reduce the
destabilizing eect of Achilles tendon vibration. Instead,
a reduction in sway velocity variability was only evident
in the last two time intervals of the vibration phase
(Fig. 4). One possible reason for this delay could be
their increased visual eld dependence conrmed by the
RFT results. The fact that vision is already up weighted
in elderly participants could delay the transition from
proprioception to vision during the anticipation of the
virtual objects to be avoided. It is already known that a
more rigid long-term up-weighting of the visual modality
is associated with a reduced ability in reweighting
multiple sensory inputs in the presence of inter-sensory
disturbances (Isableu et al., 2011). This study however
entailed the reverse experimental manipulation; visual
eld dependent individuals could not eciently exploit
the volitionally increased proprioceptive reliance induced
by body leaning to down-weight the destabilizing eect
of altered vision (i.e. sinusoidal visual eld motion) on
posture. Based on this evidence, it was expected that
older participants would benet from their overreliance
on vision to better exploit visual anticipation to downweight the perturbed proprioception. On the contrary,
older adults delay in exploiting visual anticipation
suggests a delay in dynamically shifting reliance from
proprioception to vision. One possible reason for this
delay could be their lower proprioceptive weight which
may impair their ability to rapidly detect a change in the
accuracy of the proprioceptive input. This has been
described in the literature as proprioceptive neglect
(Isableu et al., 2003), which reduces the sensitivity to
proprioceptive perturbations such as tendon vibration in
older adults (Buchman et al., 2009) possibly due to an
age-associated degeneration of peripheral receptors
(Sundermier et al., 1996; Goble et al., 2009). Indeed,
proprioceptive neglect could be supported by our data
as older participants seemed to be less perturbed by
tendon vibration in the QS task. Alternatively, volitionally
shifting sensory reliance on vision when vision is
already up-weighted might be an attention shifting
problem. Aging aects the ability to shift attentional
focus between multiple stimuli or tasks (Hawkes et al.,
2012). More generally, a failure of elderly adults to
rapidly shift sensory reliance could be related to the
decline in their cognitive motor abilities, such as motor
prediction and planning (Paizis et al., 2008; Personnier
et al., 2008; Skoura et al., 2008; Saimpont et al., 2009).
Anticipation of the collision AV events may have also
resulted in an ankle-stiening strategy due to the
imposed postural threat (Adkin et al., 2000) which in
turn, could reduce the destabilizing eect of Achilles
tendon vibration. This speculation is based on
experimental evidence indicating that the eect of
Achilles tendon vibration on body posture is attenuated
under dynamic and challenging balance conditions

(Ivanenko et al., 1999; Bove et al., 2003; Hatzitaki et al.,

2004). Moreover, during an active ankle-stabilizing
action the plantarexors contraction could attenuate the
propagation of the vibratory stimulation along the
muscle inhibiting the vibration-induced tonic reex
response (Burke et al., 1976). Nevertheless, if
increasing ankle stiness during anticipation of the
approaching objects was a strategy employed by
participants in order to compensate for the destabilizing
eects of tendon vibration, the reduction in postural
instability during the AV task should be similar, or even
greater, for the older participants. This is because
increasing postural challenge is known to result in an
age-specic ankle-stiening strategy (Carpenter et al.,
2001; Hatzitaki et al., 2005). The fact that the vibrationinduced sway velocity variability was immediately
reduced in the young but only after a delay in the
elderly participants during the AV task eliminates the
possibility that the down-weighting of proprioception
during the AV task was due to an ankle-stiening strategy.
Proprioceptive reweighting in older individuals is
possible as a function of adaptation
Elderly participants were able to exploit visual anticipation
in order to decrease the vibration-induced sway velocity
variability in the last two time intervals of the vibration
phase. This suggests that their sensorimotor system is
still adaptive and, consequently, motor function, such as
equilibrium, can be improved through appropriate
physical training. This nding supports and extends
previous research stressing the adaptive plasticity of the
aging brain (Buekers et al., 2002; Bock and Girgenrath,
2006; Hatzitaki and Konstadakos, 2007). More
importantly, it provides evidence in support of a time
consuming but ecient proprioceptive reweighting
process in aging since the vibration-induced instability is
progressively reduced as a function of adaptation
(Teasdale and Simoneau, 2001; Allison et al., 2006;
Jeka et al., 2006; Doumas and Krampe, 2010).
Re-insertion of the accurate proprioceptive input in the
post-vibration phase resulted in an initial increase in sway
velocity variability that decreased gradually to the
baseline level across successive time intervals
suggesting an eective re-adaptation process for both
groups (Fig. 5). When accurate sensory input is
restored, i.e. after the oset of tendon vibration,
reweighting has a lower priority as the body is already
able to maintain stability using the current weighting
conguration (Jeka et al., 2008). Nevertheless, this
reweighting was faster for the young than the older
participants. These observations are in agreement and
extend those of previous studies showing a longer
adaptation phase when the accurate sensory
information for controlling posture is re-inserted (Allison
et al., 2006; Jeka et al., 2006; Doumas and Krampe,
2010). This age-associated slowness can be attributed
to a reduction of the available cognitive resources and
to an overall slowness of information processing
(Salthouse, 2000) which makes the reweighting of the
available sensory information a cognitively demanding
task that is subject to prioritization and competition.

D. J. A. Eikema et al. / Neuroscience 234 (2013) 2230

CONCLUSION
This study revealed that when young individuals
anticipate visually driven collision AV, they rapidly
reduce the destabilizing eect of Achilles tendon
vibration on body posture. Contrary to the young, elderly
participants need more time to exploit visual anticipation
in order to reduce the destabilizing eect of tendon
vibration. This suggests a delay in reweighting the visual
and proprioceptive inputs possibly due to their long term
up-weighting of the visual modality. Eective sensory
reweighing in elderly adults is a time consuming process
which may have important clinical implications as this
delay may increase risk of falling in the presence of
proprioceptive perturbations. Further investigation of the
mechanisms underlying eective sensory reweighting for
controlling posture in dynamic environments may
unravel methods for improving this process in old age
though exercise and training.
AcknowledgementsThe research leading to these results has
received funding from the European Communitys Seventh
Framework Program FP7/2007-2013 under Grant agreement
number 214728-2. We would like to acknowledge the Informatics
and Telematics Institute of the Center for Research and Technology Hellas (CERTH) for providing technical assistance in the
development of the virtual environment.

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(Accepted 28 December 2012)

(Available online 7 January 2013)