Human Physiology Section of the Scientific Institute Santa Lucia and the University of Rome "Tor Vergata," 00179 Rome, Italy
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ABSTRACT |
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Ivanenko, Y. P.,
R. Grasso, and
F. Lacquaniti.
Influence of Leg Muscle Vibration on Human Walking.
J. Neurophysiol. 84: 1737-1747, 2000.
We studied
the effect of vibratory stimulation of different leg muscles
[bilateral quadriceps (Q), hamstring (HS) muscles, triceps surae (TS),
and tibialis anterior (TA)] in seven normal subjects during
1) quiet standing, 2) stepping in place
movements, and 3) walking on the treadmill. The experiments
were performed in a dimly illuminated room, and the subjects were given
the instruction not to resist the applied perturbation. In one
condition the velocity of the treadmill was controlled by a feedback
from the subject's current position. In normal standing, TA vibration
elicited a prominent forward body tilt, whereas HS and TS vibration
elicited backward trunk or whole body inclination, respectively. Q
vibration had little effect. During stepping in place, continuous HS
vibration produced an involuntary forward stepping at about 0.3 m
s1 without modifying the
stepping frequency. When the subjects (with eyes closed) kept a hand
contact with an external still object, they did not move forward but
perceived an illusory forward leg flexion relative to the trunk. Q, TS,
and TA vibration did not cause any systematic body translation nor
illusory changes in body configuration. In treadmill locomotion, HS
vibration produced an involuntary steplike increase of walking speed
(by 0.1-0.6 m·s
1).
Continuous vibration elicited larger speed increments than phasic
stimulation during swing or stance phase. For phasic stimulation, HS
vibration tended to be more effective when applied during swing than
during stance phase. Q, TA, and TS vibration had little if any effect.
Vibration of thigh muscles altered the walking speed depending on the
direction of progression. During backward locomotion, the walking speed
tended to decrease after HS vibration, whereas it significantly
increased after Q vibration. Thus the influence of leg muscle vibration
on stepping in place and locomotion differed significantly from that on
normal posture. We suggest that the proprioceptive input from thigh
muscles may convey information about the velocity of the foot movement
relative to the trunk.
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INTRODUCTION |
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Although the central networks of
coupled oscillators designated as central pattern generators
(Grillner 1981) can autonomously generate patterns of
rhythmic activity for locomotion, they are normally modulated by
supraspinal inputs and sensory signals (Armstrong 1988
;
Grillner 1981
; Lacquaniti et al. 1999
;
Orlovski et al. 1999
; Pearson et al.
1998
; Rossignol 1996
; Shik and Orlovsky
1976
). Proprioception plays a specific role in entraining the
locomotor rhythm. During fictive or real locomotion, the periodic
stretch or vibration of proximal and distal muscles can entrain or
reset the locomotor rhythm, modulating the amplitude and phase of
extensor and flexor activity (Conway et al. 1987
;
Hiebert et al. 1996
). The passive extension of the
hindlimbs involved in lifting a quiescent spinal cat triggers
air-stepping; conversely, lowering an air-stepping cat to the ground
and flexing the limbs slows or stops the rhythm. In the same animal
preparation, manually flexing one hip during walking on the treadmill
abolishes stepping in that limb, while stepping is resumed when the hip
is extended steadily to the limit that is normally reached at the end
of stance (Grillner and Rossignol 1978
). Also, the
hindlimbs of a spinal cat walking on a split-belt treadmill adapt their
cadence to each belt separately (Forssberg et al. 1980
).
Therefore sensory signals from the moving limbs have access to the
central locomotor networks to modulate walking speed, although the
overall role of peripheral feedback in the regulation of the walking
pattern may be very dependent on the type of preparation used (i.e.,
fictive locomotion or decerebrate walking or intact walking) (see
Hiebert et al. 1996
). In man, the continuous vibration
of several lower limb muscles can produce involuntary rhythmic
air-stepping of a suspended leg in horizontally lying humans
(Gurfinkel et al. 1998
).
Proprioceptive inputs are normally integrated with cutaneous, visual,
and vestibular signals giving rise to a coherent body scheme for
posture (including equilibrium maintenance) and movement (Gandevia 1996; Gurfinkel 1994
;
Lacquaniti 1997
; Massion 1992
; Soechting and Flanders 1992
; Tiemersm
1989
). One approach to probe the role of proprioception for
posture and movement consists of applying vibrations to muscles or
tendons (thereby activating mainly muscle spindle afferents)
(Bianconi and van der Meulen 1963
; Burke et al.
1976
; Goodwin et al. 1972
; Matthews and
Stein 1969
). Such stimulation has revealed some important
properties of the motor control system and of the use of proprioceptive
information. During simple voluntary arm movements, vibration of the
lengthening antagonist muscle (and not the muscle acting as a prime
mover) has been shown to be critical for accurate perception of
movement and limb position (Bullen and Brunt 1986
;
Capaday and Cooke 1981
; Cordo et al.
1995
; Inglis et al. 1991
). When applied to a
standing human subject, muscle vibration induces several effects (from illusions of ego- or exo-motion to actual body tilt) that depend on the
vibrated muscle, the sensory context and the task (Eklund 1972
; Ivanenko et al. 1999a
,c
;
Kavounoudias et al. 1999
; Lackner and Levine
1979
; Lekhel et al. 1997
; Quoniam
et al. 1990
; Roll et al. 1989b
;
Smetanin et al. 1993
). For example, shank muscle vibration evokes a prominent body tilt during quiet standing
(Eklund 1972
) or an illusion of body inclination in the
opposite direction when the trunk is fixed (Lackner and Levine
1979
). The influence of shank muscle vibration strikingly
diminishes (Ivanenko et al. 1999c
) when applied to a
subject standing on an unstable movable support.
While stimulation of supraspinal centers has been shown to have
profound influences both on posture and locomotion (see Mori et
al. 1982), the influence of proprioceptive inputs evoked by muscle vibration on human locomotion has been studied to a much lesser
extent (see, however, Gurfinkel et al. 1998
;
Ivanenko et al. 2000
). Here we report the effects of
applying mechanical vibrations to thigh and shank muscles in healthy
humans who performed the following tasks: quiet standing, stepping in
place, and walking on a treadmill at different speeds. The results
demonstrated that the most prominent effect on human locomotion was
observed during hamstring muscle vibration. We argue that the effect
may be related to the mechanisms whereby body movement relative to the
ground is represented. An abstract of these results has been published elsewhere (Ivanenko et al. 1999b
).
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METHODS |
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Experimental setup
The experiments were carried out both overground and on a
treadmill (Woodway XELG 70, Germany). Horizontal body displacement and
orientation of body segments relative to the vertical in the sagittal
plane were monitored by means of the ELITE system (BTS, Milan, Italy).
Kinematic data were digitized at 100 Hz and filtered with an optimal
low-pass FIR filter with automatic bandwidth selection. General
procedures have been previously described (Bianchi et al.
1998; Borghese et al. 1996
). Four 100-Hz TV
cameras were spaced on the recording side of the treadmill to enhance
spatial accuracy. After three-dimensional calibration, the spatial
accuracy of the system was better than 1.5 mm (root mean square). The
position of selected points on the right side of the body was recorded by attaching the infrared reflective markers to the skin overlying the
following bony landmarks (Fig.
1B): gleno-humeral joint (GH), anterior superior iliac spine (ASIS) and posterior superior iliac spine
(PSIS), greater trochanter (GT), lateral femur epicondyle (LE), lateral
malleolus (LM), and fifth metatarso-phalangeal joint (VM). ASIS and
PSIS coordinates were averaged to obtain ileum (IL) position.
Electromyographic (EMG) activity was recorded by means of surface
electrodes from the rectus femoris (RF), biceps femoris (long head,
BF), lateral gastrocnemius (GCL), and tibialis anterior (TA) using
optic fiber BTS TELEMG. EMG signals were preamplified (×100) at the
recording site, digitized, and transmitted to the remote amplifier via
15-m optic fibers (Grasso et al. 2000
). These signals
were high-pass filtered (artifact rejection was obtained by cascading 3 1st-order high-pass at 1 Hz followed by 1 1st-order high-pass at 10 Hz), low-pass filtered (200-Hz, 4-pole Bessel low-pass), and sampled at
500 Hz. Sampling of kinematic and EMG data were synchronized.
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The instantaneous velocity of the treadmill was recorded via an optical
encoder (resolution 0.005 m
s1) and controlled by a
computer at a frequency of 30 Hz. We used two different treadmill
control modes: 1) constant velocity and 2)
variable position-related velocity. In the latter mode the velocity of
the treadmill was controlled by a computer using a feedback from the
subject's position in such a way that forward displacements from the
initial position increased the treadmill velocity while backward
displacements decreased it proportionally (Fig. 1, A,
C, and D). To measure subject's position, a
light-weight stiff thread was attached to the subject (at the level of
the waist). The thread was kept in tension by a constant force (about 2 N) produced by a torque-motor (type JR24M4CH, ServoDisc, PMI, Commack,
NY). A linear potentiometer on the motor shaft measured the changes of
the subject's position (that occurred when the velocity of the subject
differed from that of the treadmill belt). Position was sampled at 30 Hz with an accuracy of 2 mm. The initial subject's position was set in
the middle of the treadmill belt. To avoid jerks, the treadmill
velocity was low-pass filtered: the transition from one velocity to
another was automatically programmed with a ramp profile of 1 m
s
2 acceleration. This
allowed dampening of fast changes in treadmill velocity due to the
natural horizontal oscillations of the body (of about ±5 cm) (see
Thorstensson et al. 1984
) during locomotion. The servo
provided an efficient and stable control of the treadmill speed in the
frequency range of 0-2 Hz. Safety circuits were incorporated in the
system. In addition, either the experimental subject or the
experimenter could stop the treadmill at any time. The feedback constant (G = 1.1; see Fig. 1) and treadmill
acceleration (1 m s
2)
were selected to make subjects feel comfortable when they changed their
walking speed. This was verified in preliminary experiments. Using such
values, the maximum attainable speed increment was 1.3 m
s
1, and no instability in
the feedback control occurred. If so required, the subjects were able
to safely increase their walking speed by about 1.3 m
s
1, up to a maximum
walking speed of 2.3 m
s
1. However, no such high
speed increments were observed following the application of mechanical vibration.
Subjects
It is known that some subjects do not show behavioral effects on
muscle vibration (Eklund and Hagbarth 1966;
Gurfinkel et al. 1998
). We performed experiments on
seven normal subjects (age 22-39 yr old, 4 males and 3 females) who
participated in earlier experiments with neck muscle vibration
(Ivanenko et al. 1999a
) and who were sensitive to
vibration from the very first application. None of the subjects had any
history of neurological disease or vestibular impairment. Informed
consent was obtained from all participants after the experimental
procedure had been explained according to the protocol of the Ethics
Committee of the Santa Lucia Institute.
Parameters of vibration
Vibrators were fastened over a muscle belly or tendon. The following muscles were tested for the effect of vibration: quadriceps (Q), hamstring (HS), triceps surae (TS), and tibialis anterior (TA).
Stimulation of leg muscle proprioceptors (1.5 mm amplitude, 80 Hz sinusoid) was performed using custom-designed electromechanical vibrators (DC motor, equipped with small eccentric rotating masses, weighted about 350 g, 9 cm long with a diameter of 4.5 cm) fixed by an elastic belt. In the case of TS muscles, vibrators were fixed to the Achilles tendons, at the level of the ankle joint. In the case of TA muscles, vibrators were fixed on the tendons of TA, 3-5 cm above the ankle joint. In the case of Q and HS muscles, vibrators were fastened over the muscle belly approximately 15-20 cm above the knee joint. In all cases, two identical vibrators were synchronized to simultaneously stimulate both legs.
We took particular care to fixate the mechanical vibrators with tight
elastic bands so that their motion at the heel impact was minimized.
The tension developed by the elastic band (3 cm wide) when wrapped
around the thigh was about 7 N
cm1, which corresponded
to a pressure of about 1 N
cm
2 (i.e., 75 mmHg acting
on the arterial vessel walls, which is about 50% of the compression
value necessary to occlude them while in standing position). To check
whether the elastic band affected the blood supply to the leg, one
subject underwent routine Doppler ultrasound measurement (Multidop,
Esaote, Italy) of blood velocity in the posterior tibialis artery. No
change following the fixation of the vibrator on the thigh was detected
in standing position. Moreover, during the experiments the vibrators
were never kept for more than 5 min, which is not long enough to cause
ischemic problems.
In two subjects we checked whether the frequency and amplitude of the vibrator was unstable during the walking cycle. We attached an infrared emitting marker on the right aspect of the vibrator on the right leg and used the OPTOTRAK (Northern Digital, Waterloo, Ontario) system (operating at 1,000 Hz with a resolution better than 0.1 mm) to measure the vibration parameters during locomotion: we found that the frequency and AM along the cycle never exceeded 10% for all vibrated muscles (Fig. 2A). The switch on/off time for 80-Hz vibration was about 400 ms with an exponential time course of the frequency change (Fig. 2B): about 200 ms was needed to reach the 50-Hz frequency.
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We evaluated the amount of vibration spreading to the antagonist muscle groups via the tight elastic band by putting an infrared marker on relevant portions of the band. During muscle vibration, oscillations of the marker placed on the band portion overlying the antagonist muscles had an amplitude of 0.1-0.2 mm (about 10% of that produced by the vibrator) orthogonal to the skin. Oscillations spred also in the direction parallel to the elastic bend (0.1-0.5 mm), but their efficiency in stimulating muscle receptors might be limited by the slip of the skin over subcutaneous tissue layers.
Protocol
Experiments were performed by the subjects with eyes open in dim ambient illumination (since they did not feel comfortable with eyes closed for more than several steps during walking on the treadmill). To record the markers located on the right side of the body, the subjects were asked to keep the arms folded on the chest. In all experiments, subjects were instructed not to resist the applied perturbation.
In the first set of experiments, continuous muscle vibration was tested in the following four conditions.
POSTURE. Subjects stood on a force platform (KISTLER 9281B) which we used to measure the displacement of the center of pressure in the sagittal and frontal directions. The centers of the heels were placed on marks 12 cm apart and the feet splayed out at approximately 30°. After 5 s of quiet standing, we applied a 6- to 8-s period of muscle vibration.
STEPPING IN PLACE. Subjects were asked to step in place. After about 5-7 s of stepping movements at a comfortable cadence (which occurred in the range 0.5-1 Hz), we delivered muscle vibration (for 7-10 s). The speed of the body displacement evoked by muscle vibration was measured by computing the slope of the regression line fitting the displacement of ilium.
TREADMILL LOCOMOTION AT CONSTANT BELT SPEED.
After 5-7 s of "steady-state" 1 m
s1 locomotion on the
treadmill, muscle vibration was applied. Changes of the walking speed on stimulation were allowed within the limits of the treadmill length.
Starting position of the subject on the treadmill could be changed so
that to use all length of the treadmill. The stimulation was switched
off when the subject approached the end of the treadmill belt. Changes
in walking speed evoked by muscle vibration gave rise to the subject's
displacement on the treadmill (relative to space) and were measured by
computing the slope of the regression line fitting the displacement of
ilium versus time.
TREADMILL LOCOMOTION AT VARIABLE POSITION-CONTROLLED BELT SPEED.
To estimate the time course of speed changes, we set up a walking
condition where the subjects were free to change their current speed on
the presence of vibration without the risk of reaching the belt bounds.
We performed the experiment in the following way: we took the subject
to the center of the treadmill belt, then we set the initial speed at
1 m s1 (in some
experiments the initial speed was set at 0.5-1.5 m
s
1 in 0.25 m
s
1 increments) and let
the subject start walking (Fig. 1A); then the treadmill
velocity was controlled proportional (by 1.1 m
s
1 per 1 m
displacement) to the changes of subject's position relative to the
starting point (Fig. 1D).
Perceived body configuration during stepping in place
In another experiment, we estimated the subjective perception of body configuration during stepping in place movements with and without vibration. We asked the subjects to hold a stable handle with their left hand and to use their right hand to point (eyes closed) with a 25-cm long stick toward the perceived location of the center of their right foot during the stance phase of stepping in place. The position of two infrared active markers attached to the stick was measured by means of a three-dimensional OPTOTRAK system. The line of the stick was extrapolated to where it intersected the ground. This subjective foot placement was compared with the real position of the foot (a 3rd marker was located on the lateral malleolus) with and without vibration.
Phasic vibratory stimulation
In addition to the standard protocol with continuous muscle
vibration, we studied the effect of phasic muscle vibration applied either in swing or stance phase during stepping in place movements and
during walking. Walking was performed at about 0.7 m
s1 (position-related mode
of treadmill velocity control). Two small mechanical footswitches
(6 × 6 mm, the load to switch them on was 3 N) were located in
the subject's shoes at the center of the heel to identify the heel
impact (beginning of the stance phase); when the heel was loaded, the
switch was on. Phasic muscle vibration was delivered in the current
step cycle according to the duration of the previous step cycle. The
signal from left and right footswitches was monitored with a sampling
rate of 200 s
1, and the
current step cycle duration was determined on-line as the time between
two successive heel impacts.
The duration of effective vibration corresponded always to 40% of the previous step cycle duration to avoid phase overlap. To overcome the delay of about 200 ms needed for the vibrator to reach 50 Hz (see Fig. 2B), we anticipated the beginning of the stimulation by 10% relative to the time of footswitch loading. Thus to trigger muscle vibration in a specific phase of the step cycle, an appropriate delay after the heel impact was programmed: 40 or 90% of the step cycle to switch on vibration in swing or stance phase, respectively. With a 40% delay, we obtained a good synchronization with the swing phase and with an additional 50% shift with the stance phase. The procedure worked because the duration of the ongoing step cycle never changed by more than 10% of the previous cycle. The left footswitch triggered the vibrator on the left leg, and the right footswitch triggered the vibrator on the right leg.
Data analysis
The body was modeled as an interconnected chain of rigid
segments: GH-IL for the trunk, IL-GT for the pelvis, GT-LE for the thigh, LE-LM for the shank, and LM-VM for the foot (Fig.
1B). The elevation angle of each segment in the sagittal
plane corresponds to the angle between the projected segment and the
vertical. The limb main axis was defined as the segment connecting GT
and LM. The gait cycle duration (T) was defined as the time
between two successive maxima of the elevation angle of the limb main
axis (Borghese et al. 1996). The stride length during
walking on the treadmill was estimated as the treadmill speed times
T averaged over several step cycles.
EMGs were numerically rectified and low-pass filtered with cutoff at 50 Hz. EMG data were time normalized over the step cycle duration
(0-100%) and then averaged over several steps. The intersegmental coordination was evaluated in position space as previously described (Borghese et al. 1996). Briefly, the changes of the
elevation angles of the thigh, shank, and foot covary linearly
throughout the gait cycle. When thigh, shank, and foot angles are
plotted one versus the others in a three-dimensional graph, they
describe paths that can be fitted by a plane computed by means of
orthogonal linear regression. The orientation of the plane relative to
the three axes is measured as the direction cosines of the normal to
the plane (i.e., the 3rd eigenvector of the covariance matrix) and
quantifies the temporal coupling among the three limb segments (Bianchi et al. 1998
).
The change of trunk, shank, and thigh orientation and center-of-pressure displacement induced by 6- to 8-s muscle vibration in quiet standing was calculated as the difference between segment orientation during the last 5 s of muscle vibration and that during the 5-s period preceding vibration. Statistical analysis (paired t-test, within-subjects ANOVA) was performed on the changes in trunk inclination and on the increment of the walking speed evoked by muscle vibration. P < 0.05 was considered significant.
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RESULTS |
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Posture
Muscle vibration during quiet standing evoked typical body
responses (Eklund 1972; Lackner and Levine
1979
), which are described in Fig.
3. Vibration of TA evoked a prominent
forward body tilt, vibration of Achilles tendons induced backward body
tilt, HS vibration elicited backward inclination of the trunk and
forward inclination of the shank due to hip extension and knee flexion,
and vibration of Q evoked no prominent postural response (Fig. 3).
Vibration of thigh muscles did not change significantly the position of the center of the body mass, whereas shank muscle vibration elicited its prominent forward (TA) or backward (TS) displacement.
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Stepping in place
When vibrating hamstring muscles during stepping in place, subjects started moving forward (Fig. 4). From a quantitative viewpoint, the effect of vibration of most muscles during stepping in place differed significantly from that obtained during quiet standing. In standing, vibration of TA and TS elicited prominent body tilt in all subjects; during stepping, vibration of these muscles evoked only small and inconsistent body displacements. Vibration of Q had little effect both on standing posture and on body displacement during stepping. On the contrary, vibration of HS muscles, which evoked knee flexion and backward trunk inclinations during standing, evoked prominent forward translation in all subjects during stepping in place. Figure 7A shows the mean speed of the evoked body displacement induced by the vibration of the four muscle groups.
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The mean speed of the evoked body displacement after HS muscle
vibration was 0.27 ± 0.16 (SD) m
s1, while in the control
(unperturbed) condition the average speed of the spontaneous subject's
displacement during 10 s of stepping in place was 0.02 ± 0.02 m s
1. We found
no evidence for the appearance of tonic muscle
activity1 in either
BF or other muscles following vibration (see Fig. 4). Forward
displacement was characterized by the changes of the phase relation
among adjacent lower limb segments. This can be appreciated in the
three-dimensional (3-D) position space (Fig. 4, bottom). Before vibration, the loops representing intersegmental coordination were close to a straight line due to the fact that the phase shift between adjacent segments was either 0 or 180°. Application of muscle
vibration did not increase the stepping frequency (stepping frequency
was 0.79 ± 0.08 s
1
and 0.80 ± 0.10 s
1
before and during HS vibration, respectively). Instead, it gave rise to
a phase shift between thigh and shank segments and a forward translation of the center of body mass. The thigh-shank-foot 3-D loops
during forward translation describe paths that can be fitted by a
planar surface (99% of variance was explained by the planar regression) (see Borghese et al. 1996
). However, motion
did not result from a transition to a natural locomotor pattern, as
reflected by the differences in the patterns of coordination described
by the 3-D gait loops of Figs. 4 and 5.
Instead, subjects continued to step in place, but the swinging foot
systematically landed in front of the standing foot.
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During stepping in place, vibration induced smaller trunk inclinations than in quiet standing, except for the case of Q vibration whose effect was equally small both during standing or stepping (Table 1).
|
Walking on the treadmill with a constant belt speed (1 m
s1)
In this protocol, the subjects underwent vibration of lower limb
muscles while they were walking on the treadmill at 1 m
s1. Changes of walking
speed on stimulation were allowed within the limits of the treadmill
length. Displacements tended to develop linearly with time; therefore
we measured the increment in walking speed as the slope of the
regression line fitting the displacement of the pelvis point versus
time during the stimulus. The stimulation was switched off when the
subject approached the end of the treadmill belt.
Among the four groups of muscles we studied, the largest increase in speed was found during vibration of HS muscles (by about 25%, Fig. 7B). Thus the relative effect of muscle vibration was roughly similar to that obtained during stepping in place. The changes in trunk inclination induced by vibration were not significantly different from those induced during stepping in place (Table 1).
Walking with position-related treadmill velocity
While walking on the treadmill with position-related belt velocity
(that is when treadmill velocity was automatically adjusted to the
subject's position), the speed increased often with a ramp-hold profile (Fig. 5) or sometimes progressively during muscle vibration. The relative magnitude of the effect of muscle vibration at the steady-state tended to be slightly larger than that during locomotion with a constant belt velocity (cf. Fig. 7, B and
C). At 1 m
s1, HS muscle vibration
increased the walking speed by 0.27 ± 0.17 m
s
1 for walking with
constant treadmill speed, whereas with the position feedback the
increase was 0.33 ± 0.17 m
s
1. For the other muscles
(Q, TA, and TS) the effect of vibration was as small as in the
condition without position feedback.
After the cessation of HS vibration, the walking speed returned
gradually to the prestimulus level (Fig. 5) or with some overshoot. The
walking speed increment induced by HS vibration was accompanied by an
increase of the stepping frequency (paired t-test,
P < 0.001) and stride length (paired
t-test, P = 0.14, not significant; however, 5 of the 7 subjects showed a significant increment). The stepping frequency was 0.82 ± 0.05 s1 before the stimulus
and 1.03 ± 0.11 s
1
during the stimulus; the stride length was 1.27 ± 0.13 m
before the stimulus and 1.32 ± 0.20 m during the stimulus.
Figure 6 shows the EMG ensemble average
of 15 gait cycles from 1 subject in 2 different steady states: during
normal walking at 1.4 m
s1 and during walking on
the treadmill with position-related belt speed when this speed was
achieved by HS muscle vibration. In all examined muscles, the EMG
activity was similar as revealed by the high correlation between the
plotted waveform pairs (Fig. 6).
|
The changes in lower limb segment kinematics displayed some amount of
interindividual variability. For example, for some subjects (as the one
in Fig. 5), there was a prominent change in the amplitude of limb
elevation angles during HS vibration. For others, these changes were
small. The 3-D gait loops representing intersegmental coordination
always evolved over a plane both with and without vibration (99% of
variance was explained by the planar regression). The orientation of
this regression plane on vibrating HS muscles also showed some
interindividual variability: for example, for four subjects (as the one
on Fig. 5), the third eigenvector of the covariance matrix decreased
with HS vibration, indicating a change in the phase relation among the
three limb segments similar to what happens during natural speed
increments (Bianchi et al. 1998); for three other
subjects, it increased. On average, there was no significant change of
the third eigenvector (0.27 ± 0.10 before HS vibration and
0.26 ± 0.12 during vibration). Thus the increment of the walking
speed induced by HS vibration in different subjects was not necessarily
accompanied by similar changes in lower limb kinematics and in the
orientation of the regression plane as during natural speed increments.
Influence of direction of progression
The effect of muscle vibration during backward locomotion was
tested in the speed range of 0.5-0.75 m
s1 (position-related mode
of treadmill velocity control). Vibrating muscles during backward
walking caused different consequences as compared with forward walking
(Fig. 7D). Vibration of HS
muscles tended to slow locomotion down rather than speeding it up. In contrast, Q vibration, which had little or no effect in forward locomotion, significantly increased the walking speed in the backward direction (paired t-test, P < 0.05). For TA
and TS muscles, the effect was tiny as in forward locomotion.
|
Influence of initial velocity
We tested whether the increment of walking speed evoked by HS
vibration depended on the initial "background" velocity. For this
purpose we used the position-related mode of treadmill velocity control
with different initial velocities (in the range of 0.5-1.5 m
s1). Figure
8 shows the results of such an
experiment. The velocity increment due to muscle vibration tended to
decrease slightly with increasing initial walking speed
(F4,24 = 2.97, P = 0.04, within-subject ANOVA).
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It is worth noting that no subject showed a transition from walking to
running. In two subjects, we tested the effect of HS muscle vibration
at an initial velocity (2 m
s1) close to or higher
than the spontaneous velocity of transition from walk to run (on
average 1.9 m s
1)
(see Thorstensson and Roberthson 1987
). Vibration
elicited a further increment of the walking speed (by 0.26 and
0.42 m s
1) but no
transition to running. However, the effect of HS vibration was not
confined to the walking mode: during running (at 2.3 m s
1), muscle vibration
also elicited a speed increment in the same two subjects (by 0.28 and
0.35 m s
1).
Continuous versus phasic HS muscle stimulation: vibration during stance and swing phase
Continuous vibration of HS muscles elicited larger speed increments than phasic stimulation during swing or stance phase both in walking and stepping in place movements (Fig. 9). HS vibration tended to be more effective when applied during swing than during stance phase (F1,6 = 11.4, P < 0.02, within-subject ANOVA for stepping in place and walking). This effect was most prominent in four subjects and less pronounced in the other three. Nobody showed a larger speed increment during HS vibration in stance phase.
|
Perceptual effects
Subjects were aware of the speed increment induced by HS vibration during stepping in place with eyes open or closed as well as during walking with eyes open. All subjects reported that they increased their speed as if "something was pushing me forward." If so required, they could make an effort to resist the imposed perturbation thus suppressing the walking speed increment induced by HS muscle vibration.
We also studied the perceptual effects during stepping in place movements when the subject (with eyes closed) kept a left hand contact with an external still object. In this condition, subjects did not move forward. During HS vibration, however, they perceived an illusory forward leg flexion relative to the trunk (Fig. 10). We characterized this illusion by estimating the subjective foot placement. In the control experiment (eyes closed, no vibration), subjects pointed (with a stick held in their right hand) on average 5 ± 4 cm ahead of the right malleolus (where the marker was placed). During HS vibration, they indicated that their feet were displaced forward relative to the control condition (by 10 ± 8 cm, range 5-30 cm). In contrast, vibration of other muscles did not elicit perceptual changes in the position of the feet relative to the trunk.
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DISCUSSION |
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The results demonstrated that a continuous muscle vibration can make subjects move forward during stepping in place or change their speed of progression during walking. In all conditions, among the muscle groups studied, the most prominent effect was found during vibration of HS muscles.
Task-dependent proprioceptive influences
The changes in posture observed during muscle vibration (Fig. 3)
are in agreement with those reported in previous studies. The posture
of the subject is modified during vibration in a manner consistent with
the brain interpreting the length of the vibrated muscle as being
"longer" than it actually is and compensating for this (e.g.,
vibration of the TA results in a forward leaning posture). However, it
is worth stressing that, in standing posture, muscle vibration induces
not local but global reactions related to the change of whole-body
orientation relative to the vertical (Eklund 1972;
Lackner and Levine 1979
; Quoniam et al.
1992
; Roll et al. 1989b
; Smetanin et al.
1993
). These changes are thought to result from a distortion of
the internal representation of the postural body scheme evoked by the
stimulation of muscle spindles (Gurfinkel 1994
;
Ivanenko et al. 1999a
; Kavounoudias et al.
1999
; Lackner and Levine 1979
; Lekhel et
al. 1997
; Massion 1992
; Smetanin et al.
1993
). The participation of local reflexes (such as
stretch-reflex) is not unequivocal since they are heavily subjected to
supraspinal modulation both in standing and locomotion depending on the
behavioral and environmental context (Capaday and Stein
1987
; Gurfinkel 1994
; Ivanenko et al.
1999c
; Nashner 1976
, 1980
).
For locomotion, the relative magnitude and even the direction of the effect of muscle vibration could differ significantly from the effect on quiet posture (Figs. 3 and 7). This rules out the explanation that changes in walking speed due to muscle vibration are merely a mechanical consequence of the postural effects (such as a shift in center of pressure relative to the current support). For example, for shank muscle vibration, there was a small effect on the walking speed in contrast to the noticeable postural changes in normal standing (Figs. 3 and 7). Therefore the role of specific muscles in affecting locomotion cannot be predicted directly from the effect seen in posture.
Also, the effect of vibration of specific muscles for locomotion cannot
be entirely predicted from the effect demonstrated during rhythmic leg
movements in lying or sitting position. Indeed, it has been found that
continuous vibration of leg muscles in humans can produce rhythmic
locomotor-like movements of the suspended leg both in forward and
backward directions (Gurfinkel et al. 1998,
1999
). It was possible to evoke rhythmic movement by
vibration of TA, TS, HS, Q, and even muscles that did not participate
in "air-stepping" (flexor digitorum brevis). The authors concluded that vibratory-induced afferent input sets into active state the central structures responsible for stepping generation. However, the
excitability of central networks, the gating of sensory information, and the role of muscle proprioception might be task-dependent. Actually, upright overground locomotion is different from the cyclic
leg movement occurring in the lying or sitting position since a number
of physiological variables are controlled in addition to the kinematic
variables. For example, the capability to control intentionally the
propulsive forces is fundamental for the adaptation of the body's
progression, both in speed and direction (Danion et al.
1997
). Equilibrium maintenance is required as well for upright locomotion.
Indeed, the increment of the walking speed induced by HS muscle
vibration (Fig. 7) may hardly be explained by a nonspecific excitation
of the central structures responsible for stepping generation, since
1) during backward locomotion, the walking speed tended to
decrease after HS vibration (Fig. 7D), 2) during
stepping in place movements, HS muscle vibration did not evoke an
increase of the stepping frequency, but it evoked a change in the phase shift among lower limb segments and a forward progression (Fig. 4), and
3) the effect of Q, TA, and TS vibration was relatively small (Fig. 7, A-C) in contrast to that observed in lying
position (Gurfinkel et al. 1998). Therefore we suggest
that proprioceptive influences are highly task dependent. The
differences among vibrated muscles in evoking rhythmic movements in
lying position (Gurfinkel et al. 1998
) and in affecting
stepping and locomotion (Fig. 7) might be related to the mechanisms
controlling walking speed and/or equilibrium during upright locomotion.
Locomotor effects of muscle vibration
The direct inertial forces applied to the moving muscle by the
vibrator's movement are unlikely to account for the effect seen on
vibration of a particular muscle as the subjects wore the vibrators in
all the recording phases. On the other hand, although the frequency and
the amplitude of the vibrator during the walking cycle were little
modulated (<10%, Fig. 2B), phasic muscle contractions and
muscle shortening or lengthening are known to affect the way spindles
and tendon organ afferents respond to vibration (Cordo et al.
1993; Prochazka 1996
; Roll et al.
1989a
). For these reasons, the firing discharge of sensory
afferents in leg muscles during the step cycle may have been complex
and phase-dependent, rather than tonic. Vibration may excite not only
receptors in the muscles under the vibrator head, but also skin
receptors and receptors in surrounding deep tissues and joints.
Yet, despite the artificial nature of the proprioceptive stimuli used
in the present study, the effect of HS muscle vibration was strong and
could thus reflect the importance of the proprioceptive input from
these muscles for human locomotion. The influences are in agreement
with earlier works on animals: imposed movement around the hip is known
to reset and entrain the rhythm during fictive locomotion in spinal and
decerebrate cats (Andersson and Grillner 1983). The
receptors signaling hip extension are probably the primary and
secondary endings of muscle spindles in hip muscles. The contribution
of receptors in hip joint is considered to be negligible because
anesthetizing hip joint receptors has no influence on the
characteristics of entrainment evoked by imposed movements around the
hip (Hiebert et al. 1996
; Kriellaars et al.
1994
; Pearson et al. 1998
).
It has been hypothesized that the degree of hip extension is monitored
by the CNS to control the instant of transition to the swing phase and
thus the timing of the stance phase (Pearson et al.
1998). However, since HS vibration should signal muscle lengthening and, hence, hip flexion, it would be expected to delay, rather than anticipate, the onset of the swing phase and, thus to
decrease the walking speed. Furthermore, HS vibration during the swing
phase or lift off was more effective than during the stance phase (Fig.
9). It is also worth stressing that, during stepping in place
movements, HS muscle vibration did not evoke an increase of the
stepping frequency; instead, vibration elicited forward progression
(Fig. 4). Therefore it is unlikely that the effects of HS vibration
seen in the present experiments can be accounted for by a mechanism
that causes an earlier transition from stance to swing phase.
While animal studies have indicated a role for input from muscle
proprioceptors in transition from stance to swing, the effects of leg
muscle vibration seen in the present studies suggest a broader role of
proprioception during human locomotion. For example, muscle
proprioception might be highly integrated in a multisensory mechanism
controlling body equilibrium during upright locomotion, which is likely
different from that during quiet posture. Continuous neck muscle
vibration can produce an increment of the walking speed as well
(Ivanenko et al. 2000). One can mention the illusory change of leg orientation evoked by HS vibration during stepping in
place (Fig. 10) and the absence of this illusion as well as the lack of
influences during vibration of Q, TA, and TS muscles. Taking into
account the illusion of leg-on-trunk flexion (Fig. 10), one could
hypothesize that HS vibration distorts the internal representation of
body configuration in such a way that the legs are upright and the
trunk is tilted forward, to which the appropriate response would be to
step forward or speed up forward gait. Furthermore, natural walking
speed increments have been shown to be paralleled by small forward
trunk inclinations (Thorstensson et al. 1984
). However,
the above interpretation is unconvincing for two reasons: 1)
the direction of the actual whole-body response is typically opposite
to that of the illusory whole-body tilt induced by the stimuli
(Fitzpatrick et al. 1994
, 1999
;
Lackner and Levine 1979
) and 2) our subjects
did never report forward trunk inclination. Instead, they perceived
forward foot displacement relative to the subjectively "stable"
trunk (Fig. 10).
Whatever the specific mechanism, the present results stress the
importance of body scheme mechanisms for the control of walking. This
would imply coherence between motor reactions to sensory stimuli and
the perceptual interpretation of such stimuli (Calvin-Figuiere et al. 1999; Fitzpatrick et al. 1994
,
1999
; Gurfinkel 1994
; Lackner and
Levine 1979
). Hamstring muscle is a bi-articular muscle
crossing the hip and knee joints. Thus a vibration-induced stimulation is compatible with either the knees being extended or the hips being
flexed. Possibly, simultaneous activation of skin receptors evoked by
muscle vibration might provide kinesthetic information about joint
angles consistent with lengthening of HS muscle (Edin and
Johansson 1995
). As a result, the internal representation of
the position of the center of body mass would be displaced behind the
supporting foot (Fig. 10, inset). To restore dynamic equilibrium in the context of this distorted representation,
compensatory moments of force would be generated resulting in a forward
acceleration of the center of body mass and in the perception of
"something pushing forward."
The differential effect of HS vibration in the swing and stance phase
(Fig. 9) and the symmetrical influences of HS and Q vibration during
forward and backward locomotion (Fig. 7) could also be related to the
mechanism of how the leg movement is represented. Vibration of the
lengthening antagonist muscle is known to be critical for accurate
perception of movement and limb position (Bullen and Brunt
1986; Calvin-Figuiere et al. 1999
;
Capaday and Cooke 1981
; Inglis et al.
1991
). For example, for stepping in place movements, hip
flexors might act as a prime motor for lifting the leg, and HS muscle
might be considered as the antagonist lengthening muscle. Thus HS
vibration could be expected to evoke larger influences. The
modification of motor synergies from forward to backward locomotion (Grasso et al. 1998
) might also account for the fact
that the proprioceptive stimulation of thigh muscles alters the walking speed depending on the direction of progression (Fig. 7).
A fundamental feature of locomotion is the continuous displacement of
the center of body mass relative to the foot contact with the support
surface. It is possible that the velocity and the position of the foot
relative to the trunk plays a key role in sensing and controlling body
movement and foot placement. Even at the level of the spinal cord,
sensory neurons in the dorsal spinocerebellar tract encode foot
location relative to the trunk (whole-limb orientation) rather than
localized proprioceptive information (Bosco et al.
1996). For geometrical reasons, foot location is more sensitive
to the changes in proximal rather than distal angles, and this factor
may account for the lack of significant influences from shank muscle
vibration. The velocity of lower limb excursion relative to the trunk
may be derived from hip muscle proprioceptors. How the increase of the
total spindle activity evoked by HS muscle vibration is interpreted and
utilized by the brain networks controlling locomotion is unknown. The
regulation of the interactions between posture and locomotion might be
critical: the increment in walking speed could represent a dynamic
adjustment caused by a distorted representation of body motion in space.
As a general conclusion, the findings highlight the importance of the proprioceptive input from muscle spindles for maintaining the steady state of human locomotion. The results demonstrated that the proprioceptive influences are strongly dependent on the task (for example, normal standing vs. locomotion vs. rhythmic leg movements in lying position) and highly specific. We suggest that proprioceptive information about the movement of the foot relative to the trunk is important for the control of the walking speed in normal locomotion.
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ACKNOWLEDGMENTS |
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The authors thank B. Bronzi and D. Prissinotti for skillful technical help and Dr. E. Troisi for color Doppler sonography measurements.
This work was supported in part by grants from the Italian Health Ministry, the Italian Space Agency, the Ministero della Universita e Ricerca Scientifica e Tecnologica, and Telethon-Italy.
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FOOTNOTES |
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1
To evaluate the amount of tonic muscle activity
induced by HS vibration on BF, we proceeded as follows. Rectified,
filtered EMGs were time normalized over the step cycle duration, and
then they were ensemble averaged over 4 steps before and during HS vibration. We calculated the mean EMG level in each of 20 consecutive 5%-wide portions of the step cycle. The lowest value was taken as an
estimate of tonic baseline components in the EMG profile. Values were
always very low both before (1.29 ± 0.23 µV, about 2% of peak
BF activity) and during HS vibration (1.58 ± 0.32 µV), the
changes being nonsignificant (paired t-test:
P > 0.08). The changes in the mean rectified EMG
activity of all muscles over the whole step cycle displayed
considerable inter-individual variability. Mean BF EMG increased in
some subjects (up to 30%, the subject shown in Fig. 10) but decreased
in others (down to 60%) such that no systematic changes could be
detected. Moreover, the changes in mean EMG activity displayed by a
given muscle during HS vibration tended to correlate positively with
those induced on the same muscle by a voluntary (no vibration) forward
stepping at similar speed (RF: r = 0.74, P = 0.06; BF: r = 0.86, P = 0.01; TA: r = 0.17, P = 0.56; GCL: r = 0.75, P = 0.05).
Address for reprint requests: Y. P. Ivanenko, Human Physiology Section, Scientific Institute Santa Lucia, via Ardeatina 306, 00179 Rome, Italy (E-mail: y.ivanenko{at}hsantalucia.it).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 8 March 2000; accepted in final form 1 June 2000.
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REFERENCES |
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