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1 Department of Experimental Medicine, Section of Human Physiology, University of Genoa, 16146 Genoa; 2 Fondazione Don C. Gnocchi, 54037 Marina di Massa; and 4 Physiological Institute, University of Pavia, and Fondazione Salvatore Maugeri, Institute of Care and Research, 27100 Pavia, Italy; and 3 Groupe Analyse du Mouvement, University of Bourgogne, 21078 Dijon, France
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Neck muscle vibration was applied to human subjects to assess the influences of neck abnormal proprioceptive input on the organization and execution of gait. Subjects walked blindfolded to a previously seen target, located straight ahead at ~4 m. Vibration was applied on the right side of the neck, both during and before walking. The variables measured were length, duration, and velocity of trajectory; relative and absolute frontal errors at target; and width of walking support base. Vibration applied during locomotion produced an undershoot of target and deviation of gait trajectory toward the side opposite to vibration. Vibration applied before locomotion produced no effect on length of trajectory but slowing of velocity and nonsystematic deviation. When vibration frequency was increased, the amplitude of the nonsystematic deviation increased. Vibration applied during or before stance trials had minor effects on body sway. Vibration before stance had no effect on the position of mean center of foot pressure, whereas vibration during stance displaced it to the side opposite to the vibrated muscle. We suggest that vibration during locomotion reduces length and velocity of trajectory because of a direct action on the locomotor centers and produces trajectory deviation related to its effect on stance. Vibration before locomotion causes a major, nonsystematic deviation from the planned trajectory, possibly connected to a disorientation of the internal references.
proprioception; orientation; posture
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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PURPOSEFUL HUMAN MOTION REQUIRES a set of conditions and capacities that allows appropriate planning, organization, and execution of a series of motor acts distributed in time and space. In voluntary movement in general, as much as in locomotion, the relative role of the central command to move and of the feedback from the evolving movement is still a matter of controversy. In principle, one can predict that the shorter the duration of a movement, the less momentous the role of the feedback, as, for instance, during a fast task of pointing to a target. On the other hand, during a slow-tracking task, such as accurately drawing a line along a predetermined path, the weight of the multifarious feedback from the periphery would be paramount.
Concurrent problems of equilibrium maintenance, intermittent leg contact with the ground, and visual control of the path further complicate the case of locomotion. It might be envisaged that, in this task, the brain organizes its neural activity with respect to a frame of external and internal references for path selection and equilibrium control, respectively, and intermittently checks the accuracy of the performance using the available feedback from the periphery. The direction of the walking trajectory depends both on its representation, which relies on a reference framework, and on the updating of the activity of the pattern generator on the basis of the input from the evolving movement. In turn, the interpretation of the "straight ahead" depends on the coordinate input from visual, vestibular, and neck receptors, which allow the brain to estimate the position of the head in space and in relation to the trunk (14, 15).
During locomotion, the cephalic segment may constitute a stabilized reference (20, 21). Even though the task imposed on the subject does not require the orientation of the head in any particular direction, head stabilization made on a geocentric reference provided by the gravitational vertical has the advantage of simplifying incoming signal processing. The vestibular system provides both the allocentric reference and direct information as to the movements of the head in space (1). This information is possibly integrated with signals from the neck at many different levels of the central nervous system, including the spinal cord (18, 19), and may contribute to the definition of the spatial relationship between head and trunk. This would allow proper direction of the action of the lower limbs along a straight-ahead path of gait. Vibration of neck muscles in human subjects induces illusions of head and visual target displacement in the absence of visual reference (2, 28) and displacement of the subjective straight ahead (26). Moreover, the velocity of treadmill walking can be modulated by vibrating the dorsal neck muscles (13).
The aim of the present investigation was to assess whether ordinate input from the neck muscles is a condition for accurate performance of straight-ahead locomotion without visual cues toward a memorized target. To this aim, muscle vibration (6) was used to produce imbalance in the proprioceptive input from the neck. Vibration was applied either before or during natural walking to identify the conditions under which the trajectory of the locomotion was more disturbed. Attention was devoted to both extent of trajectory deviation and sign of this deviation on the frontal plane with respect to the side of the neck vibration. A different action of the stimulus when applied before or during locomotion would give hints as to possible selective effects on the reference framework for locomotion steering or on the spinal circuits responsible for gait generation and execution.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects
Nine healthy young subjects (2 men and 7 women, mean age: 32.5 yr, range: 26-42 yr) volunteered for these experiments. They had no history of vestibular disorders, no signs or symptoms of cervical diseases, and no discrepancies between right and left lower limbs that could affect veering of locomotion (4).Walking
Procedure. Subjects stood on a spot, marked on the floor between their parallel feet, which were spaced 5 cm apart (starting point), and the orientation of feet, trunk, and head was aligned. They wore shoes and viewed a straight red line on the floor, which ended with a marker 4.3 m directly in front of them. This distance was empirically determined on the basis of the preliminary trials, because it permitted a comfortable execution of seven successive steps in all subjects. However, because no instruction was given to the subjects as to the required number of steps, in ~10% of trials (subjects and conditions collapsed) the number of steps to reach the target was six. At the beginning of the session, when told to "go," they walked directly to the target along the red path with their eyes open (EO) at their own preferred velocity. Subjects started walking with their right leg and ended the trial with their feet almost parallel and together.
Control conditions. The light was dimmed, and the subjects were blindfolded. Two sets of trials were performed under this condition without vibration: the subjects simply started walking as soon as they were blindfolded [eyes closed (EC)], or, in a different session, they stood quietly for a 1-min blindfolded foreperiod before starting to walk (EC1fp). The two EC and EC1fp controls were carried out to match the two vibration conditions (see sections below). Subjects repeated each of the two walking tasks five times. At the end of each trial, the blindfold was removed, and the subjects could open their eyes and see the target.
Vibration during walking. Five blindfolded walking trials were performed. Neck vibration was applied during the walking period [vibration during walking (VDW)]. The onset of the vibration signal led the subjects to start walking. The vibrator was shut off at the end of the trial when the subjects stopped walking. Two-minute rest intervals, during which the subjects were free to move around with EO, separated the trials.
Vibration before walking. On a different day, each of the subjects who participated in the former experiment performed five additional walking trials with neck muscle vibration before walking (VBW). Trials started after 1-min vibration, during which blindfolded subjects stood quietly with their face to the target. Vibration off was the signal to start walking. Again, 2 min elapsed from the end of each trial and the onset of the next trial.
Stimulation. A direct current electric motor with an eccentric fixed on the shaft, embedded in a plastic tube, produced 5-N peak-to-peak vibration at 70 Hz or 10-N peak-to-peak vibration at 100 Hz. The vibrator was applied to the right side of the cervical column, ~4 cm from the midline along the neck circumference and ~3 cm below the tip of the mastoid bone. It was fixed with tape on that spot and secured by a large elastic band that was passed dorsally around the neck, in front of the shoulders, below the axillas, and around the back. Vibration frequency was usually 70 Hz (VBW70); however, the VBW experiment was repeated in all subjects in a separate session at 100 Hz (VBW100). Note that, under the VDW condition, the vibration acted for a period of ~5-7 s, i.e., much less than under the VBW condition. Under no circumstances did the subjects report sensations of head turning or tilting in response to the vibration, nor was actual head turning or tilting observed by the experimenters.
Measurements.
At the back of each of the subject's shoes, two felt pens (red: right;
blue: left) were secured, which produced a clear-cut mark on the floor,
which was covered by a white paper layer. The location of the foot
placements was manually measured on the paper with reference to a
coordinate system centered on the starting spot (x = 0 m, y = 0 m). The errors at the target were
measured with reference to the target itself (x = 0 m, y = 4.3 m). For each trial, the
following variables were measured (Fig.
1): 1) the straight line
joining the start to the end point of the walk trajectory;
2) the time from the start to the end of the walk by means
of a chronometer; 3) the mean velocity; 4) the
relative distance between the end point and the target with respect to the frontal plane (x) and the sagittal plane (y)
(overshoot and undershoot were considered positive and negative,
respectively; right-hand and left-hand shifts were considered positive
and negative, respectively); 5) the same distances were also
taken as absolute values (independent of right or left deviation) to
get an index of the global mismatch between the intended and the
performed path (the absolute error); 6) the width of the
support base, which was the horizontal (x) distance between
one marker produced by one heel and the straight segment connecting the
markers produced by the preceding and successive strokes of the heel of
the other foot; and 7) the successive positions of the right
foot allowed the check of the linearity of the path.
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Quiet Upright Stance
The subjects who participated in the walking sessions also stood upright on a dynamometric platform (QFP Systèmes, Mougin, France) on a different day. The sampling frequency of the force exerted on three strain gauges was set at 10 Hz. The subjects were asked to stand still with their bare feet on a patterned surface at an angle of 30° and with the heels separated by 10 cm. The arms were by the subjects' sides, with EC or with EO gazing at a target placed at eye level at 1-m distance. Postural performance was measured under the following six conditions: stance with 1) EO or 2) EC without vibration; stance with 3) EO or 4) EC after 1-min vibration of the neck muscle [vibration before stance (VBS) (EO-VBS and EC-VBS, respectively)]; and stance with 5) EO or 6) EC during neck muscle vibration [vibration during stance (VDS) (EO-VDS and EC-VDS, respectively)]. Each trial lasted 51.2 s, regardless of the condition tested. The vibration (70 Hz) was applied to the same spot and side as in the walking tests. The trials were spaced by at least 3 min, during which subjects were allowed to move across the laboratory to allow recovery from possible long-lasting effects of vibration and from repetition of stance trials (27). The following variables were computed: 1) sway path or distance covered during the trial by the displacement of the instantaneous center of foot pressure (CP); and 2) mean position of the CP during the trial.Statistical Analysis
The effects of vibration on walking were assessed by ANOVA.Before ANOVA, a test on the homogeneity of the variances of the data was done (Levene's test). Two different procedures based on ANOVA were then used. Because the EO condition was represented by one trial only, the comparison of the conditions (EO, EC, EC1fp) was made by means of ANOVA for repeated measures. The differences among all EC conditions were assessed by the ANOVA, applied to all single data gathered under the EC conditions, with or without vibration, in all subjects. The post hoc Newman-Keuls test was employed to assess significant differences among EC, EC1fp, VDW, VBW70, and VBW100.
The effects of vibration on stance were assessed by a two-way ANOVA for repeated measures, where the factors were represented by the visual condition (EO, EC) and by the vibration parameters (control, VBS, VDS). The post hoc Newman-Keuls test was employed to assess significant differences among the six conditions.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Walking
Length and velocity.
There were considerable differences across subjects in the kinematics
of walking under all experimental conditions. On the average, the mean
total path lengths were not different between EO and EC (1 trial per
subject in the EO condition against the average of the means of 5 trials per subject per condition). The EC total path length was
shorter, although not significantly so, with EC1fp. Figure
2A summarizes the effect of
the vibration on the length of the straight line traced from the
starting to the end point, as averaged on the basis of all individual
EC trials with and without vibration. Length was different when all
conditions were compared (ANOVA, F = 2.868; df = 4, 220; P = 0.0242). The post hoc test showed that,
when vibration was applied during walking (VDW), path length decreased
significantly with respect to both the control condition (EC) and the
conditions with VBW (VBW70 and VBW100).
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Orientation of the walked trajectory.
Figure 3 shows examples of the gait
patterns of one subject, for five trials, obtained under four
conditions (EO, EC, VBW100, and VDW). The scatter of the
actual end point of the trajectories on the frontal (x)
plane relative to the target was measured for each trial for each
subject (the end position was evaluated as the center of the feet
support base). The scatter was negligible with EO but was somewhat
larger under the EC and EC1fp conditions. There was ample
variability in the orientation of the trajectories in the
VBW100 condition: across trials and subjects, it could lie
either on the right or on the left of the target. As a consequence, the
grand means of the scatter of the final position in the frontal plane
were not different from the EO or EC control conditions. A minor
variability in the orientation of the trajectories was present under
the VDW condition, where a systematic deviation to the left was
nevertheless observed.
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Support base. The horizontal (x) distance (see segment D in Fig. 1) between the markers produced by the heel strokes was an index of the width of the dynamic support base. The mean width of the support base was not significantly influenced by vibration, either VBW or VDW, with respect to that under the EC control conditions. Furthermore, no significant differences were found among the mean widths either across all steps or between the first and the last steps.
To assess whether the VDW produced a cumulative effect or subjects started in the wrong direction but then continued in a relatively straight path, we measured the deviation of each step as the difference between the position of the right foot at one step and that at the preceding step, for three successive steps. As a matter of fact, however, the various differences against the successive steps, subjects, and trials collapsed, showing no consistent pattern, nor was the slope of the regression line through the data points significant.Stance.
On the average, body oscillation (sway path length) was larger during
EC than EO trials under all conditions (control, VBS, VDS). A two-way
ANOVA showed in fact a significant effect of visual conditions on the
length of the sway path (EO vs. EC: F = 29.19; df = 1, 24; P < 0.0001). The vibratory stimulus, under
both VBS and VDS conditions, did produce an increase in the sway path. The VDS condition was more effective than the VBS condition. Neither effect, however, reached significance with respect to control conditions (F = 2.11; df = 2, 24;
P = 0.14). There was no interaction between visual and
vibratory conditions. Figure
5A shows the summary of the
mean sway path lengths obtained under the six conditions tested.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Neck muscle vibration produced perturbation of quiet stance, confirming previous results from the literature (22, 25). In particular, right-side vibration applied during the maintenance of stance (VDS) produced both an increase in sway and a deviation of the CP toward the side opposite to the vibration. Vibration applied before the acquisition of the stance data (VBS) had a smaller effect on sway path but no effect on mean position of the CP on the platform. The visual conditions did not obviously interfere with the vibration effects: the known effect of closing the eyes on body oscillations or position of CP (24) was not specifically changed by the neck vibration. The results observed under quiet stance condition give evidence of the effectiveness of the neck vibration procedure used in the present investigation.
Neck muscle vibration produced perturbation of gait. Vibration was effective both during (VDW) and before walking (VBW). However, the effects were different, depending on the timing of vibration. VDW induced a significant undershoot of the planned distance, with slowing of the velocity of walk, without affecting the width of the dynamic support base. VDW also produced a significant deviation of the path trajectory toward the side opposite to the neck vibration site, thus indicating a systematic effect on the orientation of the intended trajectory. Notably, the vibratory stimulation applied during walk was effective despite the relatively short stimulus duration (5-7 s, corresponding to the trial duration).
The selective side deviation induced by neck vibration administered during gait (VDW) is reminiscent of the findings obtained with VDS. Therefore, a left-side shift of the CP seems to be associated with a left-side deviation of the trajectory, perhaps as a consequence of the asymmetric neck input to brain stem or spinal centers that control balance. Preliminary findings of an investigation in which vibration was applied for a longer period during stepping in place (3) allow us to suggest that VDW did not produce an initial misdirection on the trajectory, possibly connected to the transient effect of vibration on, but a steady and systematic influence on locomotion steering. The reduction of the path length during walking with vibration (VDW) might instead be interpreted as the effect of a depressing action of the neck muscle vibration on the gait generator. The effects could be mediated either by short central circuits connecting the neck muscle afferent fibers with the mesencephalic locomotor region (17) or by direct influences on the spinal generator of locomotor pattern (11). The target undershoot, the trajectory deviation, and the (minor) velocity decrease could be the result of difficulty in integrating the conflicting sensory input and updating the ongoing motor program. During upper limb movements, tendon vibration produced under- or overshoot of a target defined in terms of elbow joint angles (7). The effects observed during gait might be the consequence of an intrusion of the abnormal neck proprioceptive input in the alternate switching from the head to foot stable frame of reference, which normally resets the pattern generator on the basis of the intermittent proprioceptive and tactile information from gait (10). A clear systematic departure of the path from the planned trajectory when directional galvanic vestibular stimulation was applied during gait has been recently reported by Fitzpatrick et al. (9). Galvanic stimulation promptly and markedly affects equilibrium maintenance during stance (8), and neck vibration produces weak but nonnegligible effects on the position of the CP. These effects might entrain balance corrections that, if operating during walk, produce some deviation of the trajectory. However, to explain the relative modesty of the side deviation shown here, it could be considered that lateralized neck muscle vibration might produce, at least in part, bilateral effects, because of the propagation through tissues and bone of the mechanical wave, much as what happens with the simple tendon tap (5).
VBW did not affect velocity of locomotion or distance walked, despite the clear-cut disorientation of gait, as shown by the large absolute error on the frontal plane (with VBW100), in the absence of a systematic deviation. A set of trials under the VBW100 condition with a shorter period of stimulus administration, similar to that used in the VDW condition, showed that some effect on the path could indeed be produced. This was a nonsystematic deviation, like with the longer stimulus duration, but the range of the errors on the frontal plane was reduced compared with the longer stimulus duration (VBW100). This finding shows that a rather brief, abnormal proprioceptive input from the neck can derange the calibration between cephalic and body segments. In passing, this finding explains why the nonsystematic error, associated with the systematic deviation produced by VDW, was larger than that observed during the control trials, thus possibly indicating an additional effect on the straight-ahead identification. Presumably, the reference framework for walking needs to be updated during, as well as before, the start of the walk. Because a few seconds are enough, some disturbance in updating can take place within a very short walk and sum up with the action producing the systematic trajectory deviation.
The absence of systematic walk deviation by VBW was consistent with the findings obtained when the vibration was administered before stance (VBS). It can be assumed that neck muscle VBW interferes with the correct reproduction of the straight-ahead direction (16) rather than with the execution of the locomotor movement. It would prevent the rehearsal of the direction of travel or induce a loss of the internal straight-ahead reference so that, from trial to trial, the direction of the blindfolded gait would be set almost randomly. Under this condition, the head would no longer be used as a stable frame of reference, possibly because of the discrepancy between the abnormal neck proprioceptive information and otolithic input. The variable error (the ample nonsystematic path deviation) indicates that neck vibration altered the whole body orienting system, which seems to be an integrating system rather than a simple relay of a proprioceptive input. One might, therefore, speculate that neck muscle vibration, administered immediately preceding the onset of walk, prevented the correct updating of the spatial reference system on the basis of the input from the vestibulum and neck proprioceptors. Otherwise, vibration would have prevented a correct "reading" of the reference parameters before planning of gait direction or would have produced a faulty integration of the inputs from the relevant receptors, thereby giving rise to an unknown reference. In this view(s), it can be suggested that planning of the gait direction implies scanning of the reference parameters immediately before the start of walking. Further investigation, during which vibration would be applied at different body levels, would confirm the specific role of the head-trunk linkage on dynamic body orientation.
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ACKNOWLEDGEMENTS |
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This research was supported by the Italian Ministry of University and Scientific and Technological Research (Progetti di Ricerca di Interesse Nazionale, 1997 and 1999) and by the University of Genova (2000).
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FOOTNOTES |
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Address for reprint requests and other correspondence: M. Schieppati, Institute of Human Physiology, Univ. of Pavia, Via Forlanini, 6, 27100 Pavia, Italy (E-mail: marco.schieppati{at}unipv.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 29 November 2000; accepted in final form 5 March 2001.
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RESULTS
DISCUSSION
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M. Bove, G. Courtine, and M. Schieppati Neck Muscle Vibration and Spatial Orientation During Stepping in Place in Humans J Neurophysiol, November 1, 2002; 88(5): 2232 - 2241. [Abstract] [Full Text] [PDF]
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: left foot; 
, right foot).
Segment D, width of the support base. Dashed lines
connecting the circles identify the half-step lengths, and the nos.
indicate the successive half steps. Straight dotted line B
joins the start to the end point of the trajectory and corresponds to
the path length. Short segment C, deviation at the end point
on the frontal plane.
