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It has been shown that the ability of humans to maintain a quiet standing posture is degraded after fatigue of the muscles at the ankle. Yet, it has also been shown that skin stimulation at the ankle could improve postural performance. In the present study, we addressed the issue of the interaction of these two effects. Subjects were tested with the eyes closed in four conditions of quiet stance: with or without skin stimulation and before and after a fatigue protocol. The skin was stimulated with a piece of medical adhesive tape on the Achilles' tendon. The fatigue protocol consisted of multiple sets of ankle plantar flexion of both legs on stool. Without fatigue, we did not observe a significant effect of the tape. With fatigue, subjects decreased their postural performance significantly, but this effect was cancelled out when a piece of tape was glued on the Achilles' tendon. This indicated that the beneficial effect of the tape was unveiled by the degraded postural performance after fatigue. We conclude that, when the muscular sensory input flow normally relevant for the postural system is impaired due to fatigue, the weight of cutaneous information increases for the successful representation of movements in space to adjust postural control.
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Degraded postural performance after muscle fatigue can be compensated
by skin stimulation
Thibaud Thedon
a,b
, Kevin Mandrick
b
, Matthieu Foissac
a
, Denis Mottet
b
, Ste
´phane Perrey
b,
*
a
Oxylane Research, 4 Boulevard de Mons, 59650 Villeneuve d’Ascq, France
b
Movement to Health, Montpellier 1 University, Euromov, 700 Avenue du Pic Saint Loup, 34090 Montpellier, France
1. Introduction
Postural performance in quiet standing is dependent on sensory
input flow [1]: degradation of visual [2,3], vestibular [4] or
proprioceptive [2–7] input flow systematically results in more
postural sway. Tendinous vibration [7], ischemia bloc [5],
anesthesia [6], muscle fatigue [2,8–11] or foam under the feet
[12] results in the same effects: on the one hand, the accuracy of
the proprioceptive information is lowered [9,11,13–15] and, on the
other hand, postural performance is lowered [2,5,7,8,10]. These
combined changes suggest that body oscillations are indeed useful
for controlling upright standing. Increasing body sway seems to be
a functional strategy to force the generation of information flow
about body stability. Stated differently, humans need to sway to
perceive the equilibrium status of their bipedal posture. In
accordance with this suggestion, Bringoux et al. [16] showed that
without sways humans are unable to perceive body tilt.
Studies using light-touch have shown an improvement of
postural performance in the elderly, diabetic and even young
subjects [12,17,18]: the digit touching an external object such as a
table resulted in a systematic drop in postural oscillations. The
interpretation of this robust empirical result is manifold. First, it is
now accepted that postural sways are controlled to facilitate the
supra-postural performance [1]. As a consequence, it might be that
the lower postural sway in light-touch condition is the result of a
different postural control, where the posture is enslaved to the
supra-postural task. A second interpretation is that the added
cutaneous stimulation could compensate for the sensory deficit of
muscle spindle and facilitate the detection of postural sway. In this
case, skin stimulation provides the central nervous system (CNS)
with a more relevant sensory inflow that in turn can lead to better
movement detection [14,21], more accurate joint position sense
[22] or better postural performance [15,23]. Finally, it can be raised
out that the digit touching an external object (such as a table)
provides an exocentric frame of reference. For instance postural
performance is better when the cutaneous stimulation is distant to
the ankle joint [19,20]. As quiet standing can be considered an
inverted pendulum with the ankle joint as the axis of rotation, it is
rather consistent that the farther the support point from the pivot
point of the pendulum, the lower the postural sways.
Several external devices have been shown to positively
influence postural stability. On the one hand, sports medicine
studies used braces or bandages at the ankle to stimulate
cutaneous sensory information and to reinforce proprioceptive
inflow [15,23]. Yet, as underlined by Bennell et al. [24], brace and
bandage have probably also reduced the capacity of subjects to
sway by a restriction of degrees of freedom. On the other hand, skin
stimulation by an adhesive tape was demonstrated to be an
Gait & Posture 33 (2011) 686–689
ARTICLE INFO
Article history:
Received 20 May 2010
Received in revised form 21 December 2010
Accepted 28 February 2011
Keywords:
Postural control
Skin stimulation
Fatigue
Light-touch
Center of pressure
ABSTRACT
It has been shown that the ability of humans to maintain a quiet standing posture is degraded after
fatigue of the muscles at the ankle. Yet, it has also been shown that skin stimulation at the ankle could
improve postural performance. In the present study, we addressed the issue of the interaction of these
two effects. Subjects were tested with the eyes closed in four conditions of quiet stance: with or without
skin stimulation and before and after a fatigue protocol. The skin was stimulated with a piece of medical
adhesive tape on the Achilles’ tendon. The fatigue protocol consisted of multiple sets of ankle plantar
flexion of both legs on stool. Without fatigue, we did not observe a significant effect of the tape. With
fatigue, subjects decreased their postural performance significantly, but this effect was cancelled out
when a piece of tape was glued on the Achilles’ tendon. This indicated th at the beneficial effect of the tape
was unveiled by the degraded postural performance after fatigue. We conclude that, when the muscular
sensory input flow normally relevant for the postural system is impaired due to fatigue, the weight of
cutaneous information increases for the successful representation of movements in space to adjust
postural control.
ß2011 Elsevier B.V. All rights reserved.
* Corresponding author. Tel.: +33 4 67 41 57 61; fax: +33 4 67 41 57 08.
E-mail address: stephane.perrey@univ-montp1.fr (S. Perrey).
Contents lists available at ScienceDirect
Gait & Posture
journal homepage: www.elsevier.com/locate/gaitpost
0966-6362/$ – see front matter ß2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.gaitpost.2011.02.027
Author's personal copy
important sensory input to conscious movement perception and to
help the CNS in localisation of which joint is in movement [13].A
tape applied in a plane perpendicular to the axis of joint movement
was found to improve movement detection [14,21] and precision
[22]. Because skin movement is restricted under the adhesive tape,
skin stretch is enhanced in the tape periphery, and this probably
allows for an easier reaching of the cutaneous discharge threshold
[21].
Following this logic, the present study wants to evaluate the
effect of skin stimulation on the stability of quiet standing using an
experimental design without supra-postural task and without
direct external spatial referential. Moreover, to enhance the
sensitivity of our protocol, we used muscular fatigue as a means
to negatively influence postural stability. If skin stimulation brings
additional sensory input flow, postural performance should be
improved, and this effect might be even stronger when muscle
function is altered by fatigue.
2. Methods
2.1. Subjects
Eight healthy young subjects (7 males and 1 female, age: 22.8
2.0 years, height:
175.8 8.6 cm, body weight: 71.0 8.4 kg) volunteered to participate in the study and
gave informed, written consent prior to the experiments. None of the subjects reported
recent lower extremity injury or a history of chronic ankle injuries in the last six
months. The study was approved by the local ethics committee and complied with the
Declaration of Helsinki for human experimentation.
2.2. Experimental protocol
Before the experimental session, each subject performed a familiarisation
session to get used to the equipment and procedures. A few days later, subjects
performed one 90 min session in a quiet room at a temperature of 20.5
0.5 8C.
Subjects were tested in two randomised conditions of quiet stance: with or without
skin stimulation, before and after a fatigue protocol. Before the fatigue protocol, 8 trials
were realized, 4 with and 4 without tape. After the fatigue protocol, 4 trials were
performed, 2 with and 2 without tape (Fig. 1). Before each post-fatigue trial, we verified
that the subject was still unable to perform more than 50% of maximal voluntary
repetition (MVR) of ankle flexors of both legs.
A quiet stance trial lasted for 51.2 s and subjects had 30 s of rest between each
trial. During stance acquisition, subjects were standing on a balance platform with
their eyes closed. All subjects wore shorts to avoid skin stimulation on legs, with the
same socks (not covering the ankles) and without shoes. The position of the feet was
standardized: the feet were oriented at an angle of 158from the sagittal midline,
with the heels 4 cm apart. Subjects’ arms were relaxed alongside of their body.
Subjects were instructed to find a comfortable position and to minimize the
amplitude of their postural sway. Data acquisition began when subjects were ready.
2.3. Fatigue protocol
The fatiguing protocol consisted of multiple sets of ankle plantar flexion of both
legs (Fig. 2). A first series of plantar flexion was realized to evaluate the MVR for
each subject. Next, subjects were requested to perform the maximal number of
series at 75% of MVR with one flexion by second. Between each series, a rest period
equal to the duration of exercise was observed. When subjects were unable to
perform more than 50% of MVR in the same time compared to the first series, the
exercise was stopped.
During the fatigue protocol, subjects stood on a footstool with their forefeet on it
(heels in space) and could touch the wall with their hands to avoid falling. Subject’s
forefeet coincided with the edge of the footstool. During the down phase it was
asked to the subjects to go below the level of the footstool to increase eccentric
muscle activity. To control that subject realized the same amplitude at each plantar
flexion (up on one’s tiptoe), two markers were positioned for the high and low
positions of the heel (Fig. 2).
2.4. Apparatus
Postural performance was evaluated with the help of a balance platform
(Me
´dicapteurs
1
, Toulouse, France) sampled at a frequency of 40 Hz. The center of
pressure (CoP) was recorded by dedicated software (Win-posturo version 1.6,
Balma, France). The following characteristics of postural performance were
calculated from the CoP data: sway area, sway path length, mean velocity, and
the antero-posterior (A-P) and medio-lateral (M-L) path length.
2.5. Skin stimulation
Skin stimulation was obtained with medical adhesive tape (3 M
TM
Transpore
TM
,
3 M, USA) glued directly on the skin. As shown in Fig. 3, a piece of tape measuring
10 cm by 2.5 cm was applied on both Achilles’ tendon in the longitudinal direction
from the calcaneus’s tuberosity. A new piece of adhesive tape was applied before
each trial of quiet stance.
2.6. Statistical analyses
The data were analyzed using Statistica software (StatSoft France 2006,
STATISTICA, version 7.1, France). Each measured variable was tested for normality
using the Shapiro–Wilk test and the Levene test for equality of variance. To test the
Fig. 2. The fatigue protocol consisted of a series of plantar flexion with controlled
timing and amplitude. Visual markers were used to check the amplitude of the
ankle movement.
Fig. 3. Location of the adhesive tape on the Achilles’ tendon.
Fig. 1. Illustration of the whole experimental protocol for one subject.
T. Thedon et al. / Gait & Posture 33 (2011) 686–689
687
Author's personal copy
assumption of normality and equality of variance, parametric test were performed.
The effects of fatigue and tape on the CoP variables were analyzed by a two-way
analysis of variance (with or without fatigue with or without skin stimulus).
When useful, HSD Tukey post hoc test was applied for multiple pairwise
comparisons. Statistical treatment included effect size assessment by calculating
partial eta-squared (
h
2
). The threshold for significance was taken at a pvalue of
0.05. In the figures, mean values are given with standard deviation (SD).
3. Results
A significant interaction between fatigue and tape was observed
for: mean velocity (F(1,7) = 9.41, p<.05,
h
2
= 0.57), total path
length (F(1,7) = 8.31, p<.05,
h
2
= 0.54), M-L path length
(F(1,7) = 13.27, p<.05,
h
2
= 0.65) and A-P path length
(F(1,7) = 5.70, p<.05,
h
2
= 0.44), expect for sway area (p= 0.06).
Post hoc analysis showed that the effect of the adhesive tape was
significant in the fatigued condition only (example for general
pattern: Fig. 4). More precisely, the tape applied on the Achilles’
tendons did not significantly influence the postural performance in
the no-fatigue condition (mean velocity p= 0.28; total path length,
p= 0.19; M-L path length, p= 0.47; A-P path length, p= 0.12; sway
area, p= 0.94).
4. Discussion
In the present study, we evaluated the effect of skin stimulation
on postural performance in a situation without supra-postural task
and without direct external spatial reference. By adding an
adhesive tape on the skin in the Achilles’ tendon region, we found
that this cutaneous stimulation had no effect on the postural
performance before fatigue, but was significantly efficient for
counteracting the degraded postural performance when the ankle
extensor muscles were fatigued.
After muscle fatigue, the contribution of muscle spindles to the
proprioceptive input flow is diminished as it was revealed by a
decrease in proprioceptive acuity evaluated by joint position sense
[9] or by the ability to detect joint movement (low back muscle
[11]). With increasing muscle fatigue, muscle spindle information
became less accurate. As a consequence, subjects use a compensa-
tory mechanism, which is necessary when the information from a
sensory channel is blurred or suppressed [2–7]: more postural
sways generate more important sensory input flow. In the present
study, total sway path length, mean velocity, M-L path length and
A-P path length increased significantly with fatigue occurrence
(+59.3%, +56.1%, +39% and +71.42%, respectively compared to the
non-fatigued condition). Similar results have been already
observed in various fatigue protocols, yet with a lower magnitude
[2,8,10]. For example, the mean sway velocity was reported to
increase by 27% after a strenuous run on treadmill [8] and by 20%
after repeated plantar flexion of both legs [2]. Similarly, the total
sway path increased by up to 45% after an ironman triathlon [10]
and by 27% after concentric ankle plantar flexion and dorsiflexion
on isokinetic dynamometer [23]. The reason for the higher
magnitude of the postural effect in the present study is likely
due to a higher degree of muscle fatigue compared to other studies
[2,8,10,23]. Moreover, our fatigue protocol relied on severe
eccentric muscle contraction when moving the body downward.
Eccentric muscle contraction is known to induce higher drop in
proprioceptive acuity than concentric contraction, when a similar
decrease in muscle force is regarded [9]. Further, it has been
proposed that the mechanism for the reduction in muscle spindle
input involves a reflex inhibition of fusimotor neurones by small
muscle afferents excited by the metabolic by-products due to the
exercise and damage to muscle fibers [25]. Noteworthy, all
subjects in the present experiment reported severe delayed onset
muscle soreness and some subjects encountered walking difficul-
ties 48 h after the protocol.
In the non-fatigued conditions, when the tape was applied on
the Achilles’ tendon, we found that subjects did not sway less
(Fig. 4).
First, this lack of significant effect is an important result when
put into perspective with the classical interpretation of a beneficial
effect of added skin information when a finger is used for a light
touch on a surface [8,10,12,19,20]. Such light-touch conditions
differ from the conditions in the present experiment: for postural
stabilisation, the light-touch imposes both an external spatial
frame of reference [29] and an adaptation of postural movements
to perform supra-postural task with accuracy [1]. For instance,
cutaneous information contributes to control the pressure
between the finger and the fixed element (e.g., table, button). In
the present experiment, skin stimulation was applied on the
Achilles’ tendon and the task was postural only. Hence, the tape
could not provide an exocentric frame of reference and the tape
could not induce a supra-postural task. As light-touch experiments
always provided an exocentric reference and/or induce a supra-
postural task, our work suggests that the postural stabilisation
effect in the light-touch conditions mainly stem from the stable
reference provided at the fingertip and the consequent redefinition
of the task in terms of supra-postural constraints.
Second, this lack of significant effect of the adhesive tape in the
non-fatigued condition is somewhat unexpected because we know
that a piece of tape applied close to a joint can improve the
detection of low velocity movements [14,21] and, more generally,
joint position sense accuracy [22]. The fact that this did not happen
in the present experiment indicates that the tape-enhanced
cutaneous input flow was not used for the control of body sway
in this experimental condition. While cutaneous receptors have a
good sensibility to movement [28], muscle spindles respond more
rapidly than cutaneous receptors [26]. So, it seems plausible that
the redundant, but delayed, cutaneous inflow did not contribute
much to the improvement of postural performance. In the non-
fatigued condition, a higher weight is given to the faster muscle
input flow, which contributes strongly to the control of quiet
standing [3].
In the fatigued conditions, when the tape was applied on the
Achilles’ tendon, we found that the postural performance was
significantly improved (Fig. 4). What mechanism(s) can account for
such a result? Because muscle spindles and cutaneous input are
able to provide similar information to the CNS [26], we argue that
the tape induced a cutaneous flow of information that the CNS used
to compensate for the less usable muscular information after
Fig. 4. Mean values for the path length of the antero-posterior (A-P) sway as a
function of ankle muscle fatigue and of the presence of an adhesive tape on the
Achilles’ tendon. Ankle muscle fatigue globally increases postural sway (p<0.05,
£
symbol). Yet, this increase is cancelled out when a tape is glued on the Achilles’
tendon (p<0.05, * symbol).
T. Thedon et al. / Gait & Posture 33 (2011) 686–689
688
Author's personal copy
fatigue. There is converging evidence that, to resolve multisensory
redundancy, the CNS has to weight the sensory information from
each channel as a function of its relevance to the context [27].In
the situation of muscle fatigue, the output of the muscle spindle is
less relevant [9,11], so the weight given to cutaneous information
could increase and thereby contribute to a better representation of
movements in space to adjust postural control.
To conclude, in the present contribution, we showed that an
adhesive tape that is adequately placed on the skin can provide
sensory information that compensate for the less accurate
muscular proprioception after fatigue. The positive results that
we obtained with young and healthy subjects could justify further
investigations, to better understand how cutaneous stimulation
could allow for enhancing postural and, maybe, dynamic
movement control. It might be that wearing elastic socks with
well designed adhesives parts would help delaying the onset of the
perceptual effects of fatigue on posture and movement control.
Finally, it is noteworthy that the results in the present study also
suggest a new and simple approach towards restoring postural
performance in case of lower limb sensory deficits. This would call
for further investigations to precisely evaluate if systems designed
after the present experiment could be beneficial for postural
stability of, for example, an elderly population that is known for a
decrease in proprioceptive acuity [30] and a daily adaptation to
this deficit.
Conflict of interest statement
The authors want to declare no conflict of interest.
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... Three variations of a unilateral exercise protocol based on concentric and eccentric muscle actions were used to induce muscle damage and DOMS was used based on previous studies with similar goals 23,33 . The dumbbell biceps curl exercise involved elbow flexion (concentric phase) and extension (eccentric phase) performed with the non-preferred arm holding a dumbbell of 3 kg for men and 2 kg for women 34 . ...
... Additional series were completed until the participant could no longer perform more than 50% of the repetitions number from the first set or there was a significant loss in the movement quality. In these cases, the protocol ended 33 . ...
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... Previous studies have indicated that muscle fatigue of different muscular regions of the body, such as ankle [2,3,[8][9][10][11][12], knee [8,10,13], hip [9,14,15], and lumbar and neck [8,16], deteriorated postural control in young adults. The effects of muscle fatigue on postural control can be explained by the following [5,17,18]: i) an alteration in proprioception (muscular, tendon, joint, and cutaneous receptors) that affects the neuromuscular junction, causing peripheral fatigue; ii) inadequate central integration of sensory information that modifies the body schema; iii) impairments in neuromuscular control and, consequently, in motor response, deteriorating the muscular contraction (i.e., decreased muscle excitability by action potential, which slows down the conduction of afferent inputs, reducing the propagation velocity of the motor output [5]). To compensate the effects of muscle fatigue during a postural task, new motor units are recruited, which requires reorganization of muscle activation and control of the movement to compensate the deficits caused by muscle fatigue [10][11][12][13][14]. Previous studies used electromyographic activity (EMG) to characterize movement strategies (e.g., postural strategies) during postural control [19]. ...
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... Thus, hypothesis H2b was not confirmed. With most CoP parameters, it was shown that the effect of fatigue on balance was in accordance with previous studies [21,22,30]. ...
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1. Thresholds for the perception of postural sway induced by gentle perturbations were determined for five normal standing subjects. In this context we understand 'perception' to mean 'able to give a subjective report'. The thresholds for the perception of movements that were equivalent to sway in velocity and amplitude were determined when the available sensory input was limited to only one, or a pair, of the vestibular, visual, and proprioceptive systems. To examine vestibular inputs alone, vision was excluded and the whole body was moved with the ankles in a fixed position. To examine visual inputs alone, the body was kept stationary and a 'room' was moved around the subjects to simulate the relative visual-field movement that occurs during standing. To limit the available sensory input to proprioception from the legs, subjects were held stationary and balanced a load that was equivalent to their own body using their ankles. In this situation, perturbations were applied to the 'equivalent body' and these could only be perceived from the resulting ankle movements. Thresholds for perceiving ankle movements were also determined in the same posture, but with the leg muscles bearing no load. 2. The thresholds for the perception of sway during standing were very small, typically 0.003 rad at a velocity of 0.001 rad s-1, and even smaller movements were perceived as the mean velocity of the sway increased up to 0.003 rad s-1. No difference was found between the thresholds for perceiving forward sway and backward sway. Eye closure during standing did not affect the threshold for perceiving sway. 3. When sensory input was limited to proprioception from the legs, the thresholds for the perception of passive ankle movements were equivalent to the thresholds for the perception of sway during standing with all sensory inputs available. When the leg muscles were relaxed, the thresholds for perceiving ankle movements increased approximately twofold. 4. The visual thresholds for perceiving movement were higher than the proprioceptive thresholds at slower velocities of movement, but there was no difference at higher velocities. 5. Both the proprioceptive and visual thresholds were sufficiently small to allow perception of the sway that was recorded when the subjects stood normally in a relaxed manner. In contrast, the vestibular thresholds were an order of magnitude greater than the visual or proprioceptive thresholds and above the largest sway movements that were recorded during normal standing.(ABSTRACT TRUNCATED AT 400 WORDS)