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Neurophysiologie Clinique/Clinical Neurophysiology (2013) 43, 237—242

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ORIGINAL ARTICLE/ARTICLE ORIGINAL

Achilles tendon vibration shifts the center


of pressure backward in standing and
forward in sitting in young subjects
Un stimulus vibratoire sur les tendons d’Achille déplace le
centre de pression en arrière en position debout et en avant
en position assise chez des sujets jeunes

G. Barbieri a,∗, A.-S. Gissot b, V. Nougier a, D. Pérennou a,b

a
Équipe Santé-Plasticité-Motricité, Laboratoire TIMC-IMAG, UMR UJF CNRS 5525, Université Grenoble 1,
38041 Grenoble, France
b
Clinique de Médecine Physique et Réadaptation, Institut de Rééducation, Hôpital Sud, CHU Grenoble, BP
338, avenue de Kimberley, 38434 Echirolles cedex, France

Received 14 September 2012; accepted 23 June 2013


Available online 17 July 2013

KEYWORDS Summary
Postural control; Objective. — An Achilles tendon (AT) vibration is known to disrupt the postural control in stand-
Verticality; ing (‘‘vibration-induced falling’’, VIF) and to backward tilt the postural vertical in restrained
Force platform; sitting position, suggesting a link between AT vibration and internal representations involved
Vibration; in postural control. A recalibration of some troubles in body orientation by oriented sensory
Proprioception manipulations could be of great clinical interest. In order to use the VIF paradigm in a procedure
suitable for a rehabilitation context, AT vibration deserves to be more investigated in sitting,
for security reasons, and first in young participants.
Method. — In 12 healthy participants (6 men/6 women; 23.3 ± 1.9 years), posturographic data
to AT vibrations (85 Hz) were recorded over 30 s standing and 40 s sitting trials.
Results. — Surprisingly, four types of differences were found between standing and sitting AT
vibrations: presence/absence of VIF and kinesthetic illusion, opposite directions of the centre of
foot pressure (CoP) displacements, different temporal profiles. In standing: VIF without kines-
thetic illusion, rapid backward shift of CoP with a peak of −54.6 ± 11.3 mm (with respect to
baseline P < 0.001) 2.8 ± 0.2 s after vibration onset. In sitting: surprising systematic forward shift
of the CoP throughout the duration of AT vibration with a maximum of 27.9 ± 18.9 mm (P < 0.05
with respect to the baseline) 19.6 ± 0.3 s after vibration onset, associated with a kinesthetic
illusion in most subjects.

∗ Corresponding author.
E-mail address: guillaume.barbieri@imag.fr (G. Barbieri).

0987-7053/$ – see front matter © 2013 Elsevier Masson SAS. All rights reserved.
http://dx.doi.org/10.1016/j.neucli.2013.06.001
238 G. Barbieri et al.

Conclusion. — The present study invalidates our idea to extend in sitting the VIF paradigm but
the unexpected results open a new window about the basic mechanisms underlying muscle
vibration effects.
© 2013 Elsevier Masson SAS. All rights reserved.

Résumé
MOTS CLÉS Objectif. — Un stimulus vibratoire appliqué sur les tendons d’Achille (TA) perturbe le contrôle
Contrôle postural ; postural en position debout (vibration-induced falling/VIF, dans la littérature anglo-saxonne)
Verticalité ; et entraîne un biais vers l’arrière de la perception posturale de la verticale en position assise
Plateforme de force ; sans possibilité de mouvement, suggérant un lien entre vibration appliquée sur les TA et mod-
Vibration ; ulation des représentations internes impliquées dans le contrôle postural. La possibilité de
Proprioception recalibrer certains troubles de l’orientation corporelle par des manipulations sensorielles ori-
entées représente un grand intérêt en rééducation clinique. La vibration appliquée sur les TA
doit donc être davantage analysée, en position assise pour des raisons de sécurité, et d’abord
avec des sujets jeunes.
Méthode. — Les données posturographiques de 12 participants sains (6 femmes/6 hommes ;
23,3 ± 1,9 ans) chez lesquels des stimuli vibratoires (85 Hz) furent appliqués au niveau des
tendons d’Achille ont été enregistrées en position debout et assise.
Résultats. — Quatre différences principales et inattendues ont été trouvées entre la position
debout et assise : présence/absence du VIF et d’illusion kinesthésique, déplacements opposés
du centre de pression (CdP), profils temporels différents. En position debout : VIF sans illusion
kinesthésique, rapide et puissant recul du CdP avec un pic à −54,6 ± 11,3 mm (comparé à la
moyenne sans vibration, p < 0,001) 2,8 ± 0,2 s après le début de la vibration. En position assise :
surprenante et systématique avancée du CdP durant toute la période de vibration avec un
maximum à 27,9 ± 18,9 mm (p < 0,05, comparé à la moyenne sans vibration) 19,6 ± 0,3 s après
le début de la vibration, associée à une illusion kinesthésique chez certains participants.
Conclusion. — L’idée d’étendre à la position assise le paradigme du VIF est invalidée. Toutefois,
les résultats inattendus obtenus ouvrent de nouvelles perspectives concernant la compréhension
des mécanismes et effets de la vibration musculaire.
© 2013 Elsevier Masson SAS. Tous droits réservés.

Introduction tilted representation of the vertical. These troubles might


be eligible to a recalibration by oriented sensory manipu-
Mechanical vibration has been widely used to modulate mus- lations in order to improve patients’ postural balance. AT
cular proprioception via Ia afferent fibers [11,16], and to vibration might be of great clinical interest for that purpose,
investigate its role in the control of erect posture. especially in elderly fallers exhibiting a retropulsion due to a
In a freely standing participant, vibration is well known PV tilted backward [15]. One idea suggested by the study of
to elicit a whole-body tilt, oriented forwards for tibialis Barbieri et al. [2] was that the VIF paradigm could be clini-
vibration and backwards for the Achilles tendons (AT) vibra- cally used to modulate the severity of the retropulsion. This
tion [1,6,9,13,14,18,21], the so-called ‘‘vibration-induced implies a methodological approach to design a procedure
falling’’ or VIF [9]. VIF was initially interpreted as the conse- suitable for a rehabilitation context for frail people show-
quence of a gastrocnemius muscle contraction in response to ing a great postural instability. For security reasons, these
an illusion of lengthening of this muscle evoked by AT vibra- procedures must be implemented in sitting.
tion [18]. This interpretation refers to a modulation of body Although the ultimate goal is to improve frail or elderly
geometry around the ankles. An alternative interpretation patients’ postural instability, a first step is to investigate
evoking a modulation of internal representations involved the VIF paradigm in sitting in young participants. Indeed
in postural control has been suggested from experiments in the VIF paradigm has never been tested in sitting. This was
weightlessness [19], and recently confirmed [2,7,20]. The the main objective of the present study. We hypothesized
study by Barbieri et al. [2] showed that AT vibration mod- that in young participants, with eyes closed, AT vibration
ulates the postural perception of vertical (PV). Using a should entail a systematic backward displacement of the
specific device wherein participants were strapped in a sit- body, associated to a backward shift of the centre of pres-
ting position to control body geometry, they showed that AT sure (CoP).
vibration induced an immediate and systematic backward PV
tilt. Recently, tendinomuscular vibration has also been used Patients and methods
to improve the spatially oriented domain of balance control,
which is impaired in amputees [8] and stroke patients [4]. Participants
Impaired lateral (lateropulsion) or sagittal (retropulsion)
body orientation are major postural problems after a stroke Twelve healthy participants (23.3 ± 1.9 years; six females
or in elderlies [3,15,17]. They may be due to a biased spatial and six males) naive with regard to the paradigm and
coordinates system referred to the vertical, and results in a purpose of the study participated in this experiment. All
Achilles tendon vibration shifts the center of pressure in young subjects 239

participants signed an informed consent as required by the After each posturographic assessment, participants were
Helsinki declaration (1964) and the local ethical committee. asked about any possible kinesthetic illusion they had expe-
rienced.
Set up
Data analysis
Postural sway was measured by two rectangular (21 × 32 cm)
force platforms (PF02, Equi, France) placed side by side. Data were analyzed in MATLAB® and statistical analy-
Each foot was placed on one of the two platforms (heels sis was performed using SPSS 14 software. Since vibratory
separated by 9 cm, toe out at 30 degrees). The trajectory stimulation of the AT induces body sway mostly in the
of the CoP under each foot was calculated from the ver- anterior—posterior direction, only this axis was considered
tical reaction forces measured by the four load cells of for data analysis. According to the experiment, different
each platform. The mean CoP displacement was then com- posturographic variables (expressed in millimeters) were
puted from the CoP displacements under each foot and calculated for each condition and participant: in stand-
from the body weight distribution between the two supports ing, the mean position of the CoP during the 10 s before
[10]. vibration onset, the backward peak reached with vibra-
Proprioceptive stimulation was delivered by two mechan- tion (calculated between the 2nd and the 3rd second of
ical inertial vibrators (VB 115, Techno concept, Cereste, vibration, due to the 2 s latency to reach the selected
France) attached to the participant’s AT with elastic bands. frequency), the forward peak reached immediately after
Vibration characteristics (frequency: 85 Hz and amplitude: vibration was stopped (calculated between the 1st and
0.85 mm) were those proposed by Roll et al. [18]. Two the 2nd second after vibration stopped), and the mean
seconds were necessary to reach the selected frequency. position of the CoP during the 12 s after vibration; in
sitting, the mean position of the CoP before vibration
(10 s), the forward peak reached with vibration (calcu-
Procedure
lated in the last second of vibration), and the mean
position of the CoP after vibration (10 s). All these values
We decided to design this study with a unique AT vibra-
were then adjusted to a normalized posturographic sig-
tion in each posture, i.e. standing and sitting, in every
nal with a mean position before vibration onset taken as
participant, for several reasons. The main reason was the
a baseline equal to 0 mm. By convention, negative values
clinical perspective we wanted to explore. The possibility
indicated a backward displacement of the CoP and posi-
of an interesting clinical effect implies an obvious effect for
tive values a forward displacement. Analyses of variance
each trial. Furthermore, due to the powerful and system-
(ANOVAs) were used for statistical comparison of the dif-
atic effect of vibration on AT in standing, on the one hand,
ferent sequences. The level of significance was set at 0.05.
and to the exploratory goal of this study in sitting, on the
Post-hoc analyses (Tukey tests) were used whenever nec-
other hand, the choice was made to study exclusively the
essary. Data are given in the form of means ± standard
primary participants’ reaction to the vibratory stimulation
deviation.
and not a mean behavior of successive trials. This allowed
eliminating possible post-effects induced by repeated AT
vibration [14,21]. Thus, only one posturographic assessment Results
per condition (one in standing and one in sitting) and per
participant was recorded in a randomized order between All participants were sensitive to vibration. The average dis-
participants. placement along the anterior—posterior axis of the CoP of
In the standing condition, participants were asked to the 12 participants in standing and sitting are represented
remain upright without resisting the possible effect of vibra- in Fig. 1.
tion with the force platform placed under the feet, barefoot, As expected in standing condition, a rapid back-
eyes closed, and arms relaxed and hanging freely along the ward tilt of the body was found, visually obvious and
body. They were instructed that the experimenter would quantified by a backward shift of the CoP (peak vibra-
protect them from falling should their balance become dis- tion = −54.6 ± 11.3 mm; P < 0.001). This peak was reached
turbed. The data were recorded over a period of 30 s, in average 2.8 ± 0.2 s after the onset of vibration. Imme-
including 10 s with no vibration, 8 s with vibration and 12 s diately after the vibration was stopped, a rapid forward
with no vibration. shift of the CoP (peak after vibration = 31.5 ± 26.5 mm) was
In the sitting condition, participants were seated on a observed, significantly different from the mean CoP after
stool with the force platforms placed under the feet, bare- vibration (4.5 ± 17.1 mm; P < 0.001). No significant differ-
foot, eyes closed and arms relaxed and hanging freely along ence was found between the CoP position before and after
the body. The participants could adjust the seat height to vibration (P = 0.939), indicating that no post-effect lasted.
feel comfortable and with instruction of having their feet In two participants, the magnitude of the VIF obliged the
entirely in contact with the force platforms. They were experimenter to slightly touch the participant in order to
instructed that the experimenter would protect them from avoid a backward fall. These trials were however taken into
falling should their balance become disturbed. They were account because the study was designed to analyze one trial
asked to not resist the possible effect of the vibration. The per participant and because this condition was analyzed just
data were recorded over a continuous period of 40 s, includ- to confirm what is well known in the literature. No partic-
ing 10 s before vibration onset, 20 s of vibration and 10 s after ipant did not report any illusion but only the perception of
the vibration stopped. the backward falling.
240 G. Barbieri et al.

Figure 1 Experimental design and mean CoP displacements in standing and sitting conditions. With each foot positioned on one
of the two force platforms (PF02, Equi, France) placed side by side and the mechanical vibrators (85 Hz) located to the Achilles
tendon, Synoptic view of the posturographic records (upper part), mean of the main CoP positions during and after vibration for
n = 12 participants (middle part) and average displacement along the anterior-posterior axis of the CoP for n = 12 participants (lower
part) in (a) standing and (b) sitting condition. The start and the end of vibration are symbolized by downward and upward arrows,
respectively. The postural responses of all participants were adjusted so that the mean value of CoP positions before the stimulation
was considered as zero millimeter. Note that the ‘‘peak’’ values (backward and forward) of the curves do not exactly correspond
to the values of the bar diagrams. Indeed a peak value given by an average curve may be different from an average of individual
peak values pointed on individual curves.

In most cases in sitting condition, the AT vibration elicited 19.6 ± 0.3 s after the onset of vibration). Once the vibration
a kinesthetic illusion of foot dorsiflexion, more globally an stopped, a progressive backward displacement of the CoP
illusion of legs’ flexion or of sliding forward of the stool. was observed and the mean position of the CoP after vibra-
Surprisingly, the vibration induced a progressive forward tion (13.9 ± 13.5 mm) was not statistically different from
shift of the CoP (peak vibration = 27.9 ± 18.9 mm, P < 0.05, that observed before vibration (P = 0.295), indicating that
Achilles tendon vibration shifts the center of pressure in young subjects 241

no post-effect lasted. Interestingly, responses to AT vibra- system (CNS) might interpret the new proprioceptive infor-
tion in standing and in sitting did not only spatially differ, mation as a lengthening of the gastrocnemius muscle and
they also had very different temporal patterns, with a much might modulate subsequently its body geometry around the
faster occurrence of the peak in standing. ankle in order to recover the initial position. This assump-
tion was supported in the present study by the existence
of kinesthetic illusions at the level of foot and leg when
Discussion participants were seated. Alternatively, an immobilization
of the vibrated segment might lead the CNS to update the
This study aimed at adapting the VIF paradigm to the sitting internal representation of the vertical resulting in a body
posture in young participants. We hypothesized that both in reorientation. From a fundamental and clinical point of
standing and in sitting conditions, AT vibration should entail view, whether muscular vibration may modulate body geom-
a systematic backward displacement of the body, associated etry, body orientation, or both depending on the context,
to a backward shift of CoP in young participants with eyes is an opened question. It could be further addressed in a
closed. more complete study using force platforms (with feet and/or
This study confirmed a finding widely reported in the lit- seat CoP information) and movement and muscular activity
erature, that is, a rapid backward fall when AT are vibrated analysis systems in standing and sitting, in parallel to mea-
in a participant standing with eyes closed (VIF), followed by surement of verticality perception with or without muscular
a rapid return to the reference position as soon as the vibra- vibration, in order to answer the following questions: which
tion stopped [1,6,9,13,14,18,21,20]. This behavior without muscles have to be vibrated? In which position? With key
illusion but with the perception of the backward falling may body segments being free or strapped? Is there any addi-
be quantified by the displacement of CoP [1,6,14,21,20], tional effect when vibration is prolonged or repeated? What
as we did here, with a peak quickly reached. We did not is more interesting: using the effect induced in one direc-
find any VIF in sitting but conversely a surprising systematic tion or using a possible after effect induced in the opposite
forward shift of the CoP throughout the duration of AT vibra- direction?
tion, associated in most cases with a kinesthetic illusion. We Regarding the experimental procedure, two points have
thus reveal four types of differences between standing and to be discussed. It is well known that in standing, a few
sitting AT vibrations: presence vs absence of VIF, absence vs seconds are necessary to reach the limits of stability and
presence of kinesthetic illusion, opposite directions of CoP to entail a backward fall. So, a prolonged time of vibra-
displacements, with very different temporal profiles. Differ- tion in this condition would not be useful. Concerning the
ent mechanisms depending on the position might encounter sitting condition, our experiment was not designed to ana-
these differences. lyze the optimal time of vibration. This experiment was
While the present study invalidates our idea to extend firstly performed in sitting in two pilot participants with a
in sitting the VIF paradigm, the unexpected result opens a time of vibration equivalent to that in standing (8 s) and
new window about the basic mechanisms underlying muscle had revealed neither a backward shift of the CoP nor a
vibration effects. At least two possible interpretations may VIF but a progressive forward shift of the CoP, with no
explain the puzzling effect. First, the forward shift of CoP steady state reached. We decided to set the experiment
may correspond to a forward shift of the centre of mass, got in sitting with a longer duration of vibration (20 s). Inter-
by the forward tilt of the trunk. This would be in contra- estingly, after 20 s of vibration, the CoP carried on its
diction with the VIF which consists in a backward whole forward shift. This might be further analysed in another
body tilt and not a forward body tilt. This argues for the experiment. As for the relatively large standard deviations
second interpretation: A plantar flexion induced a heel rise reported throughout the different CoP positions in stand-
and thus a forward shift of CoP, We cannot exclude that ing as in sitting, they were partly linked to the obvious
this effect was a consequence of a stretch reflex (vibra- individual sensibility of participants to the vibration and
tion reflex) in the calf muscles. However, it is well known also partly due to the differences in seat height and in
that vibration consequences are far more complex than a height, weight and feet size of the participants, which had
low level stretch reflex, and papers of Burke et al. [5] and not been controlled in this study. It was however notice-
Hagbarth [12] argue against this explanation. This effect able that there was little variability regarding the time of
probably refers to an adjustment of the lower limbs’ geom- occurrence of the maximum CoP displacement in stand-
etry in response to the illusion of muscular lengthening in ing.
the vibrated muscles [18]. Indeed, it was noticeable that no
illusion was experienced by participants in standing whereas
in sitting all participants reported an illusion of foot dor- Conclusion
siflexion or more globally an illusion of legs’ flexion or
of sliding forward of the stool. All together, results of a The present study invalidated the use of the VIF paradigm in
previous paper [2] and the present one showed that AT ten- sitting, but provided interesting tracks for a better under-
don vibration induces two independent but complementary standing of the effects induced by muscular vibration.
effects: one dealing with the modulation of body orienta-
tion, the other one with the modulation of body geometry.
The predominance of one mechanism on the other could be Disclosure of interest
linked to the possibility for the vibrated segment to move,
which is a much easier action to perform than to move the The authors declare that they have no conflicts of interest
whole body. Ankle articulation left free, the central nervous concerning this article.
242 G. Barbieri et al.

Acknowledgement [10] Genthon N, Rougier P, Gissot AS, Froger J, Pelissier J, Perennou


D. Contribution of each lower limb to upright standing in stroke
patients. Stroke 2008;39:1793—9.
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and in patients with motor disorders. In: Desmedt J, editor.
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