Ashton Graybiel Spatial Orientation Laboratory and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454-9110
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ABSTRACT |
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Lackner, James R., Ely Rabin, and Paul DiZio. Fingertip Contact Suppresses the Destabilizing Influence of Leg Muscle Vibration. J. Neurophysiol. 84: 2217-2224, 2000. Touch of the hand with a stationary surface at nonmechanically supportive force levels (<1 N) greatly attenuates postural sway during quiet stance. We predicted such haptic contact would also suppress the postural destabilization caused by vibrating the right peroneus brevis and longus muscles of subjects standing heel-to-toe with eyes closed. In experiment 1, ten subjects were tested under four conditions: no-vibration, no-touch; no-vibration, touch; vibration, no-touch; and vibration, touch. A hand-held physiotherapy vibrator (120 Hz) was applied ~5 cm above the malleolous to stimulate the peroneus longus and brevis tendons. Touch conditions involved contact of the right index finger with a laterally positioned surface (<1 N of force) at waist height. Vibration in the absence of finger contact greatly increased the mean sway amplitude of the center of pressure and of the head relative to the no-vibration, no-touch control condition (P < 0.001). The touch, no-vibration and touch-vibration conditions were not significantly different (P > 0.05) from each other and both had significantly less mean sway amplitude of head and of center of pressure than the other conditions (P < 0.01). In experiment 2, eight subjects stood heel-to-toe under touch and no-touch conditions involving 40-s duration trials of peroneus tendon vibration at different duty cycles: 1-, 2-, 3-, and 4-s ON and OFF periods. The vibrator was attached to the subject's leg and remotely activated. In the no-touch conditions, subjects showed periodic postural disruptions contingent on the duty cycle and mirror image rebounds with the offset of vibration. In the touch conditions, subjects were much less disrupted and showed compensations occurring within 500 ms of vibration onset and mirror image rebounds with vibration offset. Subjects were able to suppress almost completely the destabilizing influence of the vibration in the 3- and 4-s duty cycle trials. These experiments show that haptic contact of the hand with a stable surface can suppress abnormal proprioceptive and motor signals in leg muscles.
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INTRODUCTION |
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Vibrating the Achilles tendons
of a standing subject elicits backward sway and loss of balance
(Eklund 1972). Vibration circa 100-Hz stimulates the
spindle receptors of the soleus-gastrocnemius muscles thereby evoking a
tonic vibration reflex causing the muscles to shorten
(Hagbarth and Eklund
1966
).1 In
addition to a reflexive contraction of the muscles, there is a
misinterpretation of their length with the vibrated muscles being
centrally represented as longer than they actually are and the
increased length being reflected in misrepresentations of the angles of
the controlled joints (Goodwin et al. 1972
;
Matthews 1988
). For example, with bilateral vibration of
the Achilles tendons, a standing subject restrained in position will
experience forward body tilt pivoting at the ankles (Lackner and
Levine 1979
). In total darkness, such subjects, although
physically stationary, will exhibit nystagmoid eye movements with slow
phase compensatory for the apparent body motion. The sensed pivot point
of the body can also be influenced by somatosensory cues: if the
subject has a bite plate, the axis of apparent body rotation can shift
from the ankles to the head.
Somatosensory stimulation influences orientation in other situations as
well. Subjects who are free floating with eyes closed in the weightless
phase of parabolic flight maneuvers often lose all sense of body
orientation in relation to the aircraft. However, tactile stimulation
will restore a sense of orientation, e.g., pressure on their feet will
make them feel upright (Lackner and Graybiel 1983).
Moving tactile stimulation of the soles of the feet or the palms of the
hands can induce illusions of self movement in stationary, seated
subjects (Brandt et al. 1977
; Lackner and DiZio
1984
). Other evidence indicates that contact of the hand with
the rest of the body is an important element in calibrating the spatial
dimensions of the body schema (Lackner 1988
).
Somatosensory stimulation can also be used to enhance accurate spatial
localization and stabilize postural control. The oculogyral and the
autokinetic illusions are suppressed if the fixation target is attached
to the subject's hand (Evanoff and Lackner 1987;
Lackner and Zabkar 1977
). Illusions of torso rotation
induced by sinusoidally rotating the head of a stationary subject can
be suppressed if the subject is allowed to grasp a spatially fixed
handle (Gurfinkel and Levik 1993
). Standing
subjects become much more stable if they are allowed to touch a
stationary surface with their index finger at mechanically
nonsupportive force levels (Holden et al. 1987
, 1994
;
Jeka and Lackner 1994
). Such touch contact is more effective than visual cues in stabilizing balance and even allows subjects with absent labyrinthine function to balance as stably in the
dark as normal subjects (Lackner et al. 1999
). If the
finger contact reference is unstable, for example, a flexible filament, it can only serve as a regional spatial reference and attenuates sway a
limited amount (unpublished data).
The goal of the present paper was to determine the influence of finger
contact on balance in subjects being exposed to destabilizing vibration
of their leg muscles. We tested subjects in a highly demanding posture,
the heel-to-toe, tandem Romberg stance, which increases lateral
instability. To maintain balance in this posture, subjects have to keep
the vertical projection of their center of mass within the support area
defined by the width of their feet, ~10 cm. In this stance, balance
is controlled primarily by ankle everter muscles, the peroneal group,
which can exert a maximum moment of ~10 Nm before the edge of the
foot will lift up from the support surface and make it impossible to
exert further torque on the body (Winter et al. 1993).
We predicted that fingertip contact would stabilize balance during
vibration because by maintaining "precision touch" and keeping the
forces at their fingertip nearly constant, subjects would automatically
attenuate their sway.
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METHODS |
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Experiment 1: continuous leg muscle vibration
SUBJECTS. Ten right-handed college students took part after giving informed consent. They were without neurological or skeletomuscular disorders that could have influenced their balance. They ranged in age from 19 to 26 yr and in height from 162 to 185 cm.
APPARATUS. The test situation and apparatus are illustrated schematically in Fig. 1. A Kistler force platform (model 9261A) was used to measure the reaction forces generated by the feet. An ISCAN video monitoring system tracked a light-emitting diode (LED) attached to a head band worn by the subject. The "touch bar" measured the lateral (TL) and vertical forces (TV) generated by the fingertip when the subject made contact with the bar. All data were digitally sampled at 60 Hz.
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CENTER OF FOOT PRESSURE. The medial-lateral coordinates of foot pressure (CPX) were computed by Kistler hardware from FX, FY, and FZ force components detected by piezo-electric crystals in the corners of the platform.
HEAD SWAY. The medial-lateral components of head sway (HX) were computed from the movements of the head-mounted LED detected by the ISCAN video recording system after taking into account the distance of the subject's head from the camera.
FINGERTIP CONTACT FORCES.
The touch bar device for measuring forces applied by the fingertip has
been described in detail elsewhere (Holden et al. 1994). It rested on a platform riding on the Kistler force plate and was
balanced by a comparable mass on the opposite side of the platform. The
force plate detected forces applied to the touch device as well as
forces generated by the subject's feet. As a consequence, when a
subject pushed on the touch bar, the reaction forces generated at his
or her feet precisely matched the force applied to the force plate by
the base of the touch apparatus. This arrangement ensured that forces
applied to the touch bar were not erroneously interpreted as shifts of
center of pressure as would be the case if the touch bar were not
mounted on the platform. The lateral and vertical force signals from
the touch bar strain gauges were amplified and calibrated in Newtons of applied force. An auditory signal was triggered if a threshold force
level of 1 N (~100 g) was exceeded.
PROCEDURE. The subject stood in stocking feet, heel-to-toe, right foot in back without touching the left, along the central anterior-posterior axis of the Kistler force plate. This posture was chosen to enhance lateral instability of stance. The touch bar was set to the subject's right side at a comfortable height and lateral distance, the position varied only a few cm across subjects. The four conditions included: touch and no vibration (T-NV), the subject attempted to hold his or her right index finger stationary on the touch bar; touch and vibration of the peroneus longus and brevis tendons of the right leg, ~5 cm above the malleolous (T-PV); no touch and no vibration (NT-NV), the subject held his or her finger above the touch bar attempting to keep it stationary by imagining contact with a stationary spatial reference position; and no touch and peroneus tendon vibration (NT-PV), the subject held his or her finger above the touch bar attempting to maintain "contact" with an imagined spatial position while the peroneus longus and brevis tendons of the right leg were vibrated. The subjects were instructed to sway as little as possible during a trial; in trials involving finger contact, they were told to keep their finger from moving and not to set off the alarm. The left arm always hung passively at the side.
Before a trial began, the subject assumed the test posture with the forefinger above or in contact with the bar as appropriate. When the subject felt ready he or she said "go," and data collection was initiated. Subjects had their eyes closed throughout the trials. Before data collection began, several nonvibration practice trials with and without touch were given so that the subjects could feel how much force could be exerted without setting off the touch bar alarm. Trials were run in five blocks of four with each of the four conditions randomly represented in each block. The experimenter held a physiotherapy vibrator (Sears, model 793,2250) against the peroneal muscle tendons throughout each trial. In vibration trials, when the subject said "go," the experimenter turned on the vibrator and kept it on until the end of the trial. The vibrator head delivered 120 pulses/s, with an amplitude (peak to trough) of 3 mm. Stimulation at 100-120 Hz is well suited to activate muscle spindle receptors and is commonly employed to elicit tonic vibration reflexes (Goodwin et al. 1972ANALYSIS.
The heel-to-toe stance was employed to enhance medial-lateral sway. In
other experiments, we have shown that in this stance anterior-posterior
sway is small and unrelated to stimulation of the fingertip
(Holden et al. 1994; Jeka and Lackner 1994
,
1995
). Therefore, we have concentrated our analyses on
medial-lateral head and center of pressure sway measures. For each
trial, the time series of CPX and
HX were reduced to mean sway
amplitudes (MSAs) as follows
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Experiment 2: leg muscle vibration with different duty cycles
This experiment evaluated the role of finger contact in
attenuating sway when the peroneal muscle tendons were vibrated at different ON and OFF duty cycles. Subjects were
again tested in the demanding heel-to-toe posture and had their eyes
closed throughout each trial. The use of multiple periods of vibration
in a single trial creates multiple perturbations of posture in each
trial including a disturbance when the vibrator is turned on and a
rebound when it is switched off. Horak and Nashner
(1986) have shown that if subjects are exposed to repeated
translations or rotations of a platform on which they are standing,
then they soon come to anticipate the perturbation and can attenuate
its disrupting influence. We predicted that finger contact with a
stable reference would enhance subjects' ability to compensate for the
periodic muscle vibration so that in subsequent vibration cycles within the same trial they would be more stable.
SUBJECTS. Eight Brandeis undergraduate and graduate students participated after giving informed consent. All were in their 20s, and they ranged in height from 158 to 191 cm. They were without neurological or skeletomuscular abnormalities that could have affected their performance.
PROCEDURE. The experimental details and methods of data analysis were the same as in experiment 1. Eight conditions were run. All involved vibration of the right peroneal muscle tendons. Four were control conditions not involving physical contact of the index finger and four involved fingertip touch. The vibrator was held over the peroneal group by elastic tensor bandages and could be cycled for 1-, 2-, 3-, or 4-s ON and OFF duty periods (i.e., 1 s on and 1 s off, etc.) by a timing circuit that gated the vibrator starting 5 s into a trial. Trials were 40 s in duration. In touch trials, a subject attempted to keep his or her finger in the same place on the touch bar without sounding the alarm set at a threshold of 1 N. Three trials were run per condition in a randomized order.
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RESULTS |
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Experiment 1
Figure 2 presents representative trials from one subject for the four experimental conditions. All subjects showed the same patterns. CPX MSA was greatest in the vibration condition without touch (NT-PV). The next least stable condition was that without either vibration or finger contact (NT-NV). The conditions involving touch (T-NV, T-PV) were the most stable. They were not different from each other (P > 0.05); but both were significantly different from the no-touch conditions (P < 0.01, both comparisons). This means that subjects were as stable with touch and vibration (T-PV) as they were with touch without vibration (T-NV). Head (HX) MSAs showed precisely the same patterns and significance levels for comparisons between conditions. In the two conditions involving fingertip contact, subjects kept the lateral and vertical contact forces well below 1 N and did not trigger the alarm signal, finger force levels were not significantly different between these two conditions (P > 0.05). Figure 3, B and C, presents the results for the different conditions.
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The temporal relationships between the lateral forces at the fingertip (TL) and center of pressure and head sway are summarized in Fig. 3D. TL led both CPX and HX by ~250 ms in the T-NV condition. These values did not significantly change during leg muscle vibration (condition T-PV) although the lead of TL increased somewhat relative to HX. Leg muscle vibration did not affect the strength of the relationship between finger touch force and sway as can be seen from the cross-correlations of CPX and HX with TL (Fig. 3D).
The subjective reports of the participants mirror and extend the quantitative findings. In the absence of finger contact (NT-PV), subjects found the peroneal vibration extremely destabilizing. However, in the vibration condition involving finger contact (T-PV), the vibration was no longer felt to be destabilizing. Subjects could sense the vibrator against their leg but no longer felt unsteady nor as if they were moving. On average, subjects lost balance and grasped the safety railing once per trial in the no-touch, vibration condition and once every five trials in the no touch, no vibration condition (Fig. 3A). In touch conditions, there was only one instance of a subject using the safety rails in the entire experiment. When subjects held onto the safety railing this decreased their body motion and led to an underestimate of CPX MSA, especially for the no-touch, vibration condition.
Experiment 2
Figure 4 provides representative trials from a single subject for the eight experimental conditions. Figure 5 presents the mean sway amplitudes of CPX and HX across subjects within conditions. The no-touch conditions all have two to three times the MSAs of their touch counterparts and much greater standard deviations, P < 0.001 for all comparisons. All no-touch conditions have roughly comparable MSAs regardless of vibration duty cycle. In the touch conditions, the subjects were always able to maintain the finger contact force well under the 1 N level allowed.
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The reduction of each time series to a MSA actually conceals large differences in the postural responses to vibration within and across touch and no-touch conditions. These differences can be seen in Fig. 6, which presents CPX MSAs averaged across subjects and trials separately by condition for ON and OFF periods. For example, for the 1 s ON and OFF cycles, 20 1-s periods of ON and 20 1-s periods of OFF were averaged across the three trials for each of the eight subjects.
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Different patterns are apparent for the touch and no-touch conditions as vibration period is lengthened. For the 1-s duty period, the ON period of the touch condition shows a rapid leftward shift in CPX, reversing at ~0.5 s into the vibration period after peaking at ~1 cm, and then returning to the start position. The OFF period is a virtually exact mirror image of the ON period. The ON period of the no-touch condition shows a similar leftward movement of CPX, but it persists in the same direction albeit decelerating ~0.5 s into the period, peaking at ~2.5 cm of displacement as the period ends. The OFF period is a mirror image of the ON period.
For the 2-s duty cycles, the touch condition shows about a 1-cm leftward shift, reversing at 0.5 s with mirror image return to start position and maintenance near that position for the next 1 s until the period is over. The OFF period is a virtual mirror image of the ON period with a small peak sway displacement. The no-touch, ON period shows about a 2.5-cm leftward displacement peaking and reversing at ~1.5 s, with a hitch in the displacement ~0.5 s into the period. The OFF period is mirror image to the ON period.
The 3- and 4-s vibration periods are very similar for the touch conditions. The changes in medial-lateral, CPX position characteristic of the 1- and 2-s periods are greatly suppressed and only relatively small drifts from baseline are apparent with direction reversals occurring at 0.5 s and sometimes at multiples thereof. The ON and OFF periods are mirror images. The no-touch conditions show large shifts of CPX, nearly 2.5 cm, during the ON periods that reverse after ~1.5 s and then reverse again after another 1.5 s. The OFF periods are roughly mirror images of the ON periods.
Figure 7 shows the mean power frequency of CPX for the different conditions. Power peaks are present at each of the ON-OFF frequencies. The difference in sway power between the touch and no-touch conditions is huge.
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In summary, as vibration duration is increased, touch allows subjects to maintain balance without significant disruptions or changes in CPX, they remain stable throughout the ON and OFF periods. In the no-touch conditions, the subjects continue to be disrupted by the vibration at about comparable levels regardless of vibration period. The mirror image patterns exhibited in the touch conditions for the OFF periods indicate that finger contact enables active compensation for the vibration. Active compensation is clear because the CPX patterns in the touch conditions with 1- and 2-s vibration periods involve movement first in one direction then the opposite within a period. By contrast, the rebound effects in the no touch, 1- and 2-s conditions involve unidirectional shifts consistent with a passive release effect. In the ON period, there is a progressive leftward CPX shift followed by a comparable rightward shift in the OFF period. The direction reversals that are first really prominent 1.5 and 3.0 s into the 3- and 4-s no-touch, vibration conditions point to active compensations occurring although they are not as effective as the compensations achieved with finger contact in stabilizing the body.
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DISCUSSION |
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Experiment 1
Vibration of the peroneus muscles in the absence of finger contact
was very destabilizing (NT-PV > NT-NV). Our prediction that
fingertip contact would counteract vibration was borne out: when
subjects were allowed finger contact, they were as stable with peroneal
muscle vibration as they were with no vibration (T-PV = T-NV).
This is a remarkable effect further accentuated by the subjects'
reports that the vibrator no longer had any influence on their
sway so long as they concentrated on keeping their finger stationary. They also did not experience any tilt or unusual body motion when touching. The 250-ms time lead of
TL relative to
CPX has been observed in all our touch
stabilization experiments (e.g. Jeka and Lackner 1994,
1995
).
Experiment 2
Our expectation that finger contact would suppress the destabilizing effects of intermittent vibration was supported. When allowed contact, subjects were able, especially during the 3- and 4-s vibration periods, to suppress almost completely the debilitating influence of vibration. Only a modicum of improvement was apparent in the no-touch conditions: the subjects were unable to develop anticipatory compensations to counteract either the primary effects of vibration or the mirror image release effects.
General discussion
Our first experiment demonstrated that finger contact could
completely suppress the instability induced by continuous vibration of
the peroneal muscles and the illusory motion induced by such vibration.
Subjects were as stable during vibration when allowed finger contact as
when allowed touch in the absence of vibration. They were more stable
in both of these conditions than in the control condition in which
there was neither finger contact nor vibration. The extent of
instability in the no-touch vibration conditions is underestimated
because periodically the subjects had to push against the safety
railing to regain balance. In the touch trials, subjects were always
able to keep their finger contact force below the 1 N level permitted.
Under optimal conditions, 1 N of force at the fingertip would be able
to absorb at most 3% of the sway energy. The actual sway reduction in
our touch conditions was ~70%. Detailed experimental and modeling
data for sway attenuation by finger contact are presented in
Holden et al. (1994) and Rabin et al.
(1999)
.
Our second experiment showed for a range of vibration duty periods that finger contact can greatly suppress the consequences of vibration. This effect is dramatic at the longer vibration periods. It indicates that the nervous system is able to anticipate what the consequences of vibration will be and to implement compensations that nearly cancel these effects. These compensations apparently cannot be fully implemented when finger contact is absent because the no-touch conditions show disruptions at all duty cycles though partial compensation is present for the 3- and 4-s ON-and-OFF periods.
In the touch trials, the extent of compensation increased with period duration even though the order of conditions was randomized. This is likely because after the subjects had received several trials, they recognized that all ON vibration and OFF vibration periods within that trial would be identical to the first ones in the trial and that all trials were the same length. This allowed them to anticipate the consequences of subsequent vibration periods and subsequent OFF periods within a trial. Touch contact enabled subjects to model very effectively the 3- and 4-s duty periods; however, in the absence of finger touch, effective compensatory innervations to restore equilibrium were not possible. The same predictive information about vibration sequencing was present in both touch and no-touch trials, but, in the absence of touch, subjects were unable to anticipate the nature of the disruption in sufficient detail to counteract it.
The touch conditions thus implicate a potential role for internal
models, both inverse and forward (cf. Miall and Wolpert 1996), involving detailed monitoring of arm configuration and fingertip force patterns and anticipated consequences of vibration and
compensatory motor innervations on body position. Limb position must be
monitored quite precisely for finger contact to have such strong
stabilizing effects on posture or it would not be possible for the
nervous system to distinguish between changes in fingertip contact
forces resulting from postural shifts and from shifts in arm
configuration relative to the torso (cf. Rabin et al.
1999
).
A natural way to interpret our findings is in terms of "precision
touch," in analogy to the concept of "precision grip" introduced by Johansson and Westling (1987). They showed that the
nervous system is extremely sensitive to micro-displacements at the
fingertips. When an object being held between the thumb and index
finger starts to slip, changes in grip strength just adequate to
suppress slip occur "automatically" (Johansson
1991
). Our results indicate that one finger can make precision
contact with a surface and that whole-body, postural musculature can be
automatically marshaled to preserve that contact. This is a
nonconscious mobilization in which the task goal of maintaining light
contact is conscious but the details of implementation are not. It is
likely that the nervous system can automatically modulate the postural
apparatus to achieve precision contact or grip with any mobile part or
combination of parts of the body.
Control is dependent on regulating the somatosensory input at the fingertip, which under the experimental conditions, is the relevant receptor region. Adjustments of arm and leg muscles are made as appropriate to minimize changes at the fingertip, and the configuration of body segments between the fixed points of the feet and fingertip is monitored. Vibrating the ankle muscles alters balance and finger contact, but automatic adjustments are made to alleviate alterations in finger force thereby stabilizing posture. That this would be the case should not be surprising because tool use and manipulation are a quintessential human activity. In every day life, we constantly reach for and manipulate objects and tools while adjusting our postural muscles to maintain precise control at the relevant effector surface, be it the fingertips or the tip of a screw driver blade. Attention is attuned to the hand or the tool, not the postural musculature involved in achieving the control.
An important feature of our experiments is that the hand has
representational priority in control of spatial orientation. For
example, in other studies we have shown that if a blindfolded subject
is standing and maintaining precision touch with a surface, then if
unbeknownst to the subject the surface is oscillated at low amplitude,
he or she will become entrained and sway at the same frequency as the
surface. The subject will perceive the finger contact surface to be
stationary and not perceive his or her body sway even though it would
be supra-threshold in the absence of finger contact (Jeka et al.
1997, 1998
). In yet other studies, we have shown that the hand
has representational priority in affecting the perceptual
representation of both body orientation and body configuration
(Lackner 1988
). The present experiments show the importance of the hand in allowing the CNS to monitor and model the
destabilizing effect of leg muscle vibration on postural control in
order both to regain stability and to prevent destabilization. These
observations have obvious significance for developing rehabilitation paradigms for individuals with balance deficits. The importance of the
hand in spatial control may relate to the enormous amount of cortex
devoted to the sensory and motor aspects of hand function relative to
that assigned to the other parts of the body.
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ACKNOWLEDGMENTS |
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We thank Dr. Joel Ventura for technical advice.
This research was supported by National Aeronautics and Space Administration Grants NAG9-1037 and NAG9-1038.
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FOOTNOTES |
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Address for reprint requests: J. R. Lackner, Ashton Graybiel Spatial Orientation Laboratory, MS033, Brandeis University, Waltham, MA 02454-9110 (E-mail: lackner{at}brandeis.edu).
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.
1
Vibration of other than soleus-gastrocnemius and
tibialis anterior postural muscles does not always lead to postural
responses consistent with shortening of the vibrated muscles. Instead
the opposite response may be seen because of distributed postural adjustments driven by supraspinal mechanisms. Eklund
(1972) provides an excellent analysis. Vibration elicits
tonic vibration reflexes when the postural muscle is unloaded and not
being used in supportive stance.
Received 7 February 2000; accepted in final form 19 July 2000.
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REFERENCES |
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