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1Neurological Science Research Center, Department of Physiology, University of Montreal and Center for Multidisciplinary Research in Rehabilitation (CRIR), Rehabilitation Institute of Montreal, Montreal; 2Jewish Rehabilitation Hospital, CRIR, Laval, Quebec; and 3School of Rehabilitation Sciences, University of Ottawa, Ottawa, Ontario, Canada
Submitted 24 August 2006; accepted in final form 4 April 2007
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ABSTRACT |
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INTRODUCTION |
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; Ma and Feldman 1995). The trajectories remain invariant even if the hand movements are produced to remembered targets, i.e., in the absence of vision (Pigeon et al. 2000). When the trunk is moving, the influence of trunk motion on the hand trajectory is minimized by appropriate compensatory modifications of the arm joint angles, compared with the situation when the trunk is motionless (Adamovich et al. 2001). These angular modifications in trunk-assisted reaching are called compensatory arm movements or compensatory arm–trunk coordination. When trunk motion is either free or blocked in randomly occurring trials, the invariance of hand trajectory is maintained by using or excluding the compensatory coordination, respectively. When pointing is produced to targets beyond the arm's reach, the influence of the trunk motion on the hand trajectory is initially fully compensated, but when the arm approaches the reaching limits, the gain of the compensatory coordination is attenuated, allowing the trunk to contribute to the hand movement extent and direction (Rossi et al. 2002).
Adamovich et al. (2001) addressed the question of whether the compensatory arm–trunk coordination relies on an anticipatory strategy by making modifications of arm joint angles depending on the prediction of the presence or absence of trunk motion in the approaching trial. They analyzed trunk-assisted pointing movements to targets placed within arm's reach. The trunk motion was prevented in comparatively rare and randomly selected trials. In this situation, the anticipatory strategy would be ineffective because of the high probability of errors in anticipation and, as a consequence, frequent movement errors. Subjects had no difficulty in maintaining the same hand trajectory regardless of the trunk condition, implying that the compensatory coordination in trunk-assisted reaching may not rely on anticipation. Adamovich et al. (2001) also found that centrally programmed compensatory reactions triggered on-line (i.e., when the trunk moves during the current trial) would be too late to account for the invariance of the hand reaching trajectory. Thus neither anticipatory nor triggered compensatory central commands, but rather sensory (proprioceptive, cutaneous, and/or vestibular) feedback resulting from trunk motion may underlie the compensatory modifications in arm joint angles that maintain the same hand trajectory despite changes in the number of degrees of freedom involved in the pointing task.
The involvement of vestibulospinal pathways in trunk-assisted reaching tasks was previously demonstrated in studies using galvanic vestibular stimulation (GVS; Bresciani et al. 2002a; Day and Reynolds 2005; Mars et al. 2003). It was concluded that these pathways can induce short-latency changes in ongoing whole body movements (Fitzpatrick et al. 1994; Ivanenko et al. 2000; Lackner 1988). Similar conclusions were derived from studies of passive trunk rotations during arm reaching (Bresciani et al. 2005; Guillaud et al. 2006). These studies analyzing the role of the vestibular system in reaching movements did not exclude the possibility that proprioceptive feedback (conveyed to arm motoneurons, for example, from hip muscles during trunk flexion in the study by Mars et al. 2003) in isolation or in combination with the vestibular system underlies the compensatory arm–trunk coordination. Addressing this issue, Tunik et al. (2003) found that deafferented patients who lost kinesthetic and cutaneous sensitivity below the nose (large neuropathy of myelinated peripheral sensory fibers) but not vestibular sensitivity were able to maintain the hand-pointing trajectory irrespective of whether trunk movement was involved. They hypothesized that vestibular signals evoked by the head motion following the trunk flexion play a major role in the initiation, maintenance, or modification of the compensatory arm–trunk coordination. In the present study, we tested the suggestion following from this hypothesis that the compensatory action can be impaired in patients with vestibular deficits, despite the availability of proprioceptive–cutaneous feedback. With this purpose, we investigated trunk-assisted pointing movements in patients with unilateral vestibular lesions (UVLs) resulting from surgical resection of an acoustic neuroma. Testing also involved the task of maintaining the same hand position when the trunk moved (stationary hand task).
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METHODS |
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).
A battery of the following clinical tests was performed in the patients participating in our study (Table 1). Dynamic visual acuity (DVA) was evaluated using the protocol suggested by Dannenbaum et al. (2005). It measured the difference in the number of lines that the subject was able to read in the usual E-chart for visual acuity when the head was passively rotated (±20° at 1.5 Hz) and when it was motionless. Scores < –1 indicate a deficit in DVA and imply a decrease in the gain of the vestibuloocular reflex (VOR). The Halmagyi impulse test (HIT; Halmagyi et al. 2003) measured movement of the eyes during a discrete passive rapid rotation of the head from 30° of cervical rotation to the midline position. A positive response was recorded if the participant could not preserve the gaze direction (following a deficit in the VOR), so that, to restore the direction, a single catch-up saccade toward the side of the lesion was produced (Low Choy et al. 2006).
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The impact of dizziness on daily life [dizziness handicap inventory (DHI)] was evaluated based on 25 questions (Jacobson and Newman 1990). Scores ranged from 0 (no dizziness) to 100 (severe dizziness).
Experimental procedures
Subjects were seated on a stool with the back near an electromagnet attached to the wall behind them (Fig. 1). They wore a harness with an electromagnetic plate fastened posteriorly at the level of the scapulae. The plate was locked to the electromagnet, keeping the subject in an upright position at the beginning of each trial. Subjects also wore liquid crystal glasses (Translucent Technologies, Plato S2 Spectacles) allowing blocking of vision simultaneously with an auditory signal to move.
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25 cm from the sagittal midline, at an angle of –40°). With the hand at the starting position, shoulder horizontal and elbow angles were respectively about 0 and 100° for the ipsilateral and 65 and 115° for the contralateral target. Before each trial, subjects kept the index finger near the appropriate target. In response to a "go" signal (tone) from a computer, subjects had to produce a trunk flexion at the hip level to lean the trunk forward (displacement 20–30 cm at the level of sternal notch) while holding the hand motionless. Vision was blocked simultaneously with the "go" signal. After a short stop at a final position, subjects returned the trunk toward its initial position and vision was restored. In 70% of the 40 trials in each experiment, the electromagnet was inactivated simultaneously with the auditory signal, allowing the trunk to move. In the remaining 30% of randomly selected trials, the electromagnet remained locked after the auditory signal, blocking the trunk in the initial vertical position. To prevent fatigue, subjects could rest 10–15 s between trials by holding the hand on the knees. To discourage subjects from anticipating experimental conditions in forthcoming trials, they were told that the perturbation would be applied randomly and that they should produce arm and trunk movements in a stereotyped way in all trials. Before the experiments began, subjects practiced making the movements (five trials) with vision and without perturbations.
The same ipsi- and contralateral targets and trunk arrest paradigm were used in reaching experiments 3 and 4. Before each trial, subjects kept the index finger near a starting target—the LED embedded in a board placed on the knees. The LED was located on the middle sagittal line, about 15 cm from the frontal surface of the trunk. The starting configuration of the arm with the trunk in the upright position was the same for both final targets (the shoulder horizontal abduction and elbow angles were about 20 and 95°, respectively).When the LED indicating the starting target was on ("ready" cue), subjects lifted the hand with the fingers 1–2 cm above the LED. The target to which the hand should move was still visible. In response to the sound signal, when vision was blocked, subjects had to move the hand to the remembered target while simultaneously leaning forward the trunk and head together irrespective of whether the trunk was blocked, as in experiments 1 and 2. Subjects were asked to move the hand toward the target with a single stereotypical movement, without corrections at the end of it. After a short delay at the final position, they moved the arm and trunk back to the initial position. Vision was restored when the subjects returned to the starting position. Subjects were instructed not to anticipate the trunk condition or make corrections to touch the target. It is known that vestibular deficits are compensated by vision (e.g., Borel et al. 2002). By asking our patients to move to remembered targets we had the opportunity to analyze vestibular deficits not confounded by the visual compensation. Without vision of the hand, patients were also deprived of knowledge of results and could not use visual or tactile feedback to correct movement errors (Adamovich et al. 2001).
Experiments started after a brief practice session in which subjects made three reaching movements to one or another target with vision, but without trunk arrest. No knowledge of results or feedback regarding movement errors was given to the subjects throughout experiments. The order of experiments was counterbalanced across subjects.
Every subject was tested with his/her dominant hand. Results with nondominant hand were also collected in four UVL patients (targets 1 and 2 were respectively rearranged). In healthy subjects, reaches with dominant and nondominant arm were previously compared (Tunik et al. 2003) in the same age group and showed similar compensatory reactions to trunk arrests.
Data recording and analysis
Movements of the arm and trunk were recorded using an optoelectronic three-dimensional (3D) motion-analysis system (Optotrak, sampling rate 100 Hz; 4 s/trial). Markers (infrared LEDs) were placed on bony landmarks: tip of the index finger, head of the ulna (wrist), lateral epicondyle (elbow), right and left acromion processes (shoulders), and sternal notch (trunk).
In four healthy and two vestibulo-deficient subjects we additionally placed a marker in the midline of the forehead to determine whether the head–trunk angle changed during the trunk movements or when the latter was blocked, even though subjects were instructed to flex their trunk by leaning the trunk and head together, as a single rigid body. Head–trunk angle was evaluated by computing the angle between the vector joining the head and sternal markers and the plane defined by two shoulder and one sternal marker. We also recorded EMG activity of four neck muscles (left and right sternocleidomastoides and trapezius) to determine whether there were reflex responses in these muscles when the trunk was blocked. There was a small intermittent change in the head–trunk angle not exceeding 2.7°. There were no significant changes in the EMG activity associated with the trunk perturbation.
The coordinates of the index and sternal markers were used to compute, respectively, hand (endpoint) and trunk trajectories, as well as sagittal and tangential velocities (Adamovich et al. 2001). The other markers were used to determine principal joint angles. The elbow flexion–extension angle was calculated based on the product of two vectors, one joining the markers on the wrist and lateral epicondyle and the other joining the markers on the lateral epicondyle and right acromion process (shoulder). To compute the shoulder flexion–extension and horizontal abduction–adduction angles, we first determined the trunk plane defined by three markers—two on the shoulders and one on the sternal notch. Then we determined two planes that were orthogonal to each other and to the trunk plane. When the trunk was vertical, one of these planes resembled to the sagittal and the other the horizontal plane. The shoulder flexion–extension and horizontal abduction–adduction angles were defined as the angles between the corresponding projections of the epicondyle–shoulder vector on these planes and the trunk plane (Adamovich et al. 2001). Compensatory arm movements are based on coordinated changes in all these angles, rather than on changes in a single angle (Adamovich et al. 2000, 2001). To indirectly evaluate this coordination, the sum of all three angles was also computed and compared in different conditions in each group of subjects.
For data averaging, kinematic data were aligned with respect to their onsets, which was determined for each trial when tangential velocity rose to >5% of its peak value (Adamovich et al. 2001). The fingertip and trunk mean trajectories (±SD) and velocities were computed and represented graphically. Interjoint coordination was characterized by the mean (±SD) relationship between the elbow and shoulder horizontal angle (angle–angle diagrams). The hand trajectories in blocked-trunk and free-trunk trials from each experiment were compared. The divergence of the trajectories in the two types of trials was identified as the point when the mean trajectory from the blocked-trunk trials left the mean ± SD zone for the free-trunk trials. The divergence of other variables (joint angles and velocity profiles) in the two types of trials was identified in a similar way.
If not compensated, the motion of the trunk resulting from flexion at the hip joints would shift the hand position, both in sagittal horizontal and vertical directions. Therefore we specifically focused on the trunk-related changes in the hand position and trajectory in the sagittal direction. The degree of compensation was characterized by coefficients [gains (g)] in each experiment
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). These errors were not the focus of our study. To exclude the confounding influence of the vision-dependent systematic errors on the gain measurements, coefficients sa and s were evaluated by computing the deviation in the final positions of the index finger and sternal markers in blocked-trunk trials from the respective positions in free-trunk trials. With the same purpose, subjects were instructed to reproduce the same final hand position in each trial, rather than precisely reach the target.
Note that when sa = 0, the endpoint maintains or reaches the same position irrespective of whether the trunk was moving. In this case the influence of trunk motion on the hand position is fully compensated and g = 1. In contrast, when there is no compensation, sa = s and thus g = 0 (Pigeon and Feldman 1998; Rossi et al. 2002).
Statistical analysis
Because of differences in variances between groups, Mann–Whitney U test and Kruskal–Wallis ANOVAs were used to compare the results of age-matched controls and UVL patients. To compare the results of individual patients with the control group, an adapted version of the t-test for individual observations was used (Jolicoeur 1998), with n – 1 = 6 number of degrees of freedom (n is the number of controls). Spearman correlations were also used for statistical estimations. The significance level in all tests was P < 0.05.
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RESULTS |
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The trunk movement amplitudes (patients: mean = 0.27 ± 0.05 m; controls: mean = 0.27 ± 0.05 m), maximal tangential velocities (patients: mean = 0.52 ± 0.28 m/s; controls: mean = 0.46 ± 0.17 m/s), and deviation of the trunk motion from the sagittal direction (patients: mean = 2.2 ± 5.0°; controls: mean = –0.4 ± 3.6°) were not significantly different between the two groups of subjects (P > 0.1). In patients, the lesion side did not influence the trunk displacement direction (P = 0.9). Figure 2 illustrates the results from one UVL patient and one control subject. Instructed to keep the hand stationary near the ipsilateral or contralateral target while moving the trunk forward, control subjects were able to reduce the influence of trunk motion on the hand position, with mean gains of 0.87 ± 0.08 for ipsilateral and 0.84 ± 0.10 for contralateral target. Thereby the average hand displacement in the horizontal plane did not exceed 6.6 cm (mean = 2.7 ± 2.1 cm) for the ipsilateral target and 7.5 cm (mean = 3.7 ± 2.1 cm) for the contralateral target. On average, in control subjects, the forward trunk bending could, if not compensated, shift the hand vertically by 16.3 cm downward, whereas the actual vertical hand displacement was about 2.5 cm.
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Fig. 5).
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In contrast to control subjects, maximal sagittal hand velocities in five UVL patients in free-trunk trials were significantly closer to those of the trunk (range = 0.09–0.87 m/s, mean = 0.31 ± 0.31 m/s, P < 0.05). In yet another patient (patient 6), the tangential hand velocity was also significantly higher (0.22 m/s, P < 0.05) compared with controls (range = 0.08–0.14 m/s, mean = 0.11 ± 0.02 m/s). Quantitatively, in patients 1 and 2, sagittal and tangential velocities of the hand and trunk in free-trunk trials were similar, implying that 60–100% of the trunk velocity was transmitted to the hand (Fig. 6). In patients 3–6, the effect of trunk motion was smaller (35–60% of trunk velocity was transmitted to the hand). Unlike the others, patient 7 moved the hand in the direction that was opposite to that of trunk movement, showing an overcompensation. For the group of patients and both targets, the trunk tangential velocities in patients were transmitted to the hand more than in control subjects (U = 24, P < 0.01). In the blocked-trunk trials, sagittal hand velocities of six UVL patients (range = 0.01–0.14 m/s, mean = 0.03 ± 0.04 m/s) were usually smaller and not distinguishable from the residual trunk velocity. For the blocked-trunk condition, sagittal hand velocity was significant only in patient 1 (about 0.5 m/s for both targets).
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TRAJECTORIES.
As in previous studies of reaching movement in control subjects (Adamovich et al. 2001), the unexpected arrest of the trunk motion did not significantly influence the hand trajectory (Fig. 4A). Only in two of seven control subjects, did the hand trajectories diverge at a late phase of movement (after 75–90% of total displacement). Healthy subjects tended to reach somewhat further in the sagittal direction in the free-trunk trials. The difference between the mean final positions in the two types of trials did not exceed 6.4 cm (mean = 4.8 ± 1.2 cm) for the ipsilateral and 8.1 cm (mean = 5.7 ± 3.3 cm) for the contralateral target.
In contrast, all UVL patients except patient 7 were unable to preserve the hand trajectory in the two types of trials. The trajectories began to diverge after the hand covered 50–60% of the movement distance. The trajectory was shorter in the blocked-trunk trials by 9–17.5 cm (mean = 13.5 ± 3.9 cm), corresponding to 21–48% (mean = 31 ± 10%) of the total hand movement distance. The hand trajectory deviated in the sagittal direction by 4–16 cm (mean = 11 ± 3 cm), transferring the final hand position closer to the body and by 5–13 cm (mean = 8 ± 3 cm) closer to the midline in the frontal direction when the trunk was blocked. For the two targets, the reaching deficits in patients were similar (U = 10, P > 0.05) and did not vary with the side of lesion or hand dominance (Kruskal–Wallis, H1,7 < 1, P > 0.2). In pointing to the two targets, the compensation gains in the group of patients were significantly less than in controls (Fig. 3, U = 30, P < 0.05). Six patients were unable to preserve the hand trajectory when the trunk moved. Mean variability in the performance characterized by the SD of gains (average for both targets) was larger in UVL patients than in control subjects (U = 9, P < 0.05).
INTERJOINT COORDINATION. To preserve the hand trajectory when the trunk moved, control subjects appropriately changed arm joint angles (Table 3). For both targets, with an increase in forward trunk bending, elbow flexion increased, thus preventing an overshoot of the target.
In UVL patients, angle–angle diagrams (Fig. 5) showed abnormal patterns of interjoint coordination. Most patients significantly overshot the ipsilateral target when the trunk moved (Fig. 4), either because of a minimal elbow flexion (patients 1, 4, and 5) and/or a 35–50% reduction in the shoulder abduction (patients 1–3). Compared with control subjects, the changes in shoulder flexion angle tended to be smaller in the group of UVL patients (U = 11, P = 0.085).
For the contralateral target, control subjects combined a shoulder horizontal adduction with an elbow extension if the trunk sagittal displacement was relatively small (<15 cm) or with an elbow flexion when trunk displacement was >15 cm, to avoid overshooting. In patients, overshooting in free-trunk trials was associated with smaller elbow flexion that did not compensate for the substantial trunk movement (in patients 2, 4, 5, and 6). Patients 1, 5, and 6 also abnormally produced shoulder horizontal abduction instead of adduction (P < 0.05).
In free-trunk trials, to prevent the contribution of sagittal trunk motion to the hand position or trajectory, it was necessary to make appropriate compensatory modifications in the arm joint angles (compensatory arm–trunk coordination; see INTRODUCTION), compared with the situation when the trunk was blocked. The first sign of compensation was the divergence, after a certain latency, in arm joint angles between free-trunk and blocked-trunk conditions. For all control subjects and UVL patients, the interjoint coordination profile in blocked-trunk trials initially followed that in free-trunk trials and began to diverge after the trunk mean velocities started diverging. Based on the time of the trunk velocities divergence, we found that the shortest latency for the onset of compensatory changes in the arm joint angles in control and UVL subjects were similar (60–80 ms; U = 22, P > 0.5, latency range: 60–180 ms, mean = 94 ± 34 ms for controls; range: 80–240 ms, mean = 107 ± 33 ms for patients). To compensate for the trunk arrest and reach the ipsilateral target, an elbow extension and a smaller shoulder horizontal abduction were required (see Table 3, Controls). In patients, a shorter hand trajectory in blocked-trunk trials was associated with a significant shoulder horizontal adduction instead of abduction (in patients 1 and 2, P < 0.05) or a smaller elbow extension (in patients 3 and 6). For the contralateral target, control subjects produced a shoulder horizontal adduction and elbow extension. A significantly shorter trajectory was observed in six patients, associated with reduced elbow extension (in patients 1, 3, and 6) and/or reduced shoulder adduction (in patients 1, 5, and 6, P < 0.05).
VELOCITY PROFILES.
Hand movement durations and peak velocities were similar in the two groups of subjects, for both targets (duration: in free-trunk trials, mean = 1.00 ± 0.13 s for controls and 0.89 ± 0.16 s for patients; in blocked-trunk trials, 1.01 ± 0.17 s for controls and 0.80 ± 0.16 s for patients; hand peak tangential velocities: in free-trunk trials, 1.22 ± 0.27 m/s for controls and 1.35 ± 0.38 m/s for patients; in blocked-trunk trials, 1.18 ± 0.31 m/s for controls and 1.19 ± 0.40 m/s for patients). In control subjects, hand sagittal velocity profiles for the two trunk conditions were practically identical, for both targets. Statistically, for 90% of the movement duration, the mean velocity curve of the blocked-trunk trials did not leave the ± SD zone computed for the free-trunk trials. On average, the hand peak velocities for the two trunk conditions differed <10% (mean difference = 7 ± 4%). Although subjects were instructed to move the hand and trunk simultaneously, the trunk usually continued to move 100–200 ms after the hand stopped moving, as was also observed in other studies (Adamovich et al. 2001; Pigeon and Feldman 1998). In addition, the hand reached its peak velocity significantly before the trunk. The delay between the two events was not different for the two groups of subjects (range: 61–304 ms, mean = 170 ± 2 ms for controls; range: 74–268 ms, mean = 153 ± 61 ms for patients; U = 25, P > 0.5).
In UVL patients, hand sagittal velocity profiles in the two trunk conditions clearly diverged (Fig. 6, bottom right). In addition, these profiles were more variable than in control subjects (Fig. 6, compare bottom right and bottom left). In five of seven patients, the velocity profiles began to diverge at the acceleration phase of movement. In six patients, the sagittal hand movement in the blocked-trunk trials finished earlier than in the free-trunk trials. Also, in patients, hand maximal velocity tended to be reduced in the blocked-trunk trials (in six patients, by 13–53%, mean = 26 ± 13%) and, in five patients, the hand velocity peaks in the two trunk conditions, in contrast to those in control subjects, were not synchronized. For both targets, the reduction of hand maximal sagittal and tangential velocities in patients relative to controls during blocked-trunk conditions was significant (Kruskal–Wallis, H1,28 = 7.34, P < 0.05). In six patients, in free-trunk trials, the hand velocity profile resembled the trunk velocity profile, implying a low degree of compensation. In patient 5, movements were segmented in blocked-trunk trials, i.e., had two peaks in the velocity profiles rather than one peak typically observed in other control subjects and UVL patients. The hand sagittal displacement was shorter in patients 1–6 compared with the control group when the trunk was blocked (patients: by 48 ± 12%; controls: by 11 ± 10%; U = 3, P < 0.01 for both targets).
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DISCUSSION |
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The present study confirmed previous findings of compensatory changes in the arm joint angles that maintain the same hand trajectory despite changes in the number of body segments involved in trunk-assisted reaching in the absence of vision in healthy subjects (Adamovich et al. 2001). We extended these findings to the stationary hand task in which healthy subjects had to keep the hand motionless when the trunk was moving. A deviation of the gain from 1.0 in our study (range 0.71–0.99 for healthy subjects) indicates that the absence of vision worsens the trunk–hand compensatory coordination (Pigeon et al. 2000). In experiments on humans and animals, vision can indeed improve motor actions and even help restore postural equilibrium affected by vestibular lesions (e.g., Borel et al. 2002; Pavlova et al. 2004).
Most UVL patients preserved some, although reduced, capability of switching from one pattern of arm interjoint coordination to another when the trunk condition changed from trial to trial. They thus tended to meet the task demand of maintaining the same hand position or trajectory in respective tasks regardless of the trunk condition. In principle, both healthy subjects and UVL patients could prepare, in a feedforward way, appropriate patterns of arm interjoint coordination and trigger one or another pattern depending on anticipation of the trunk condition in each approaching trial. Because the trunk condition changed randomly from trial to trial, this anticipatory strategy could result in frequent movement errors and variability (Adamovich et al. 2001). The errors could be minimized if subjects triggered an appropriate coordination pattern after recognizing the trunk condition during each trial. The latency of such condition-dependent triggered reactions would be substantially greater (300–500 ms; see Adamovich et al. 2001) than the observable latency of angular modifications in our study. Therefore it seems unlikely that UVL patients or healthy subjects used feedforward strategies in our tasks (with a possible exception for patient 7; see following text). Trunk bending was accompanied by proprioceptive and cutaneous signals resulting from motion at the hip joint in free-trunk trials or from the increasing pressure from the harness on the frontal surface of the thorax in blocked-trunk trials. However, these proprioceptive and cutaneous signals were equally available in both healthy and UVL subjects and could not be responsible for the substantial differences in the degree of compensation in these two groups of subjects. Most likely, the intact vestibular system could provide effective compensatory reactions neutralizing the influence of the trunk motion in healthy subjects. The remaining side of the vestibular system could also enable UVL patients to produce, albeit insufficient, compensatory movements. Our data thus reinforce the suggestion (Adamovich et al. 2001; Bresciani et al. 2002b, 2005; Guillaud et al. 2006; Mars et al. 2003) that vestibular signals play a major role in adapting arm movement to maintain the same motor action regardless of the presence or absence of trunk motion. This conclusion is also supported by the finding that the loss of proprioceptive and cutaneous sensation does not prevent deafferented patients from making adequate compensatory reactions during trunk-assisted reaching (Tunik et al. 2003): the vestibular system, although mildly affected in deafferented patients (Cooke et al. 1985; Forget and Lamarre 1994; Tunik et al. 2003), is sufficient for this.
The vestibulospinal pathways project directly or indirectly, by spinal interneurons, to motoneurons of arm muscles (e.g., Büttner-Ennever 1999) and thus these pathways may provide compensatory modifications of arm movements related to trunk motion. As in a previous study (Tunik et al. 2003), healthy subjects began compensatory modifications of arm joint angles after a minimal delay of about 60 ms. Similar delays in arm motor responses to vestibular stimuli were reported when sudden passive trunk rotations were produced during a tracking task (Guillaud et al. 2006). Our estimates of the delay were based on kinematics and therefore somewhat exceeded (in particular, because of electromechanical delay) the delay values (30–50 ms) reported for EMG responses to GVS in arm muscles (Baldissera et al. 1990; Britton et al. 1993; Mars et al. 2003). The response delay of muscles of the back and leg to GVS (60–75 and 100–120 ms, respectively) is bigger as a result of the difference in the time of propagation of vestibulospinal signals (Ali et al. 2003; Ardic et al. 2000).
Trunk-assisted reaching is not a unique motor action in which task-specific compensations involving the vestibular system come into play. A classic example is the VOR compensating for head rotation to maintain gaze stability. The gain of the compensation is attenuated when the head rotation must contribute to gaze shifts (Guitton 1992; Johnson and Sharpe 1994). Our findings suggest that the vestibular compensations inherent in the VOR and arm–trunk coordination serve a similar purpose: to preserve the constancy of perception and action in the external space during head or whole body motion (Pigeon et al. 2000; Rossi et al. 2002).
It is known that there exists a spinal system of interlimb interaction mediated by proprioceptive and cutaneous signals (Alstermark 1987; Grillner et al. 1971; Jankowska et al. 2005; Minor et al. 1990; Ten Bruggencate et al. 1969). Nevertheless, it is not this but the vestibular system that appears to play a leading role in guiding the compensatory arm–trunk coordination. The situation is similar for the eye–head coordination during gaze fixation: in the VOR, compensatory eye movements could, in principle, be driven by proprioceptive signals activated during head rotation. However, it is vestibular and not neck proprioceptive signals that guide compensatory eye movements when the head is rotated. There may be a fundamental reason for such a preference related to the fact that gaze, hand fixation, or reaching movements are produced in frames of reference associated with the environment. In contrast, proprioceptive and cutaneous signals deliver kinesthetic information in a local, body-centered frame of reference. Therefore sensory systems that deliver information in reference to the environment—the visual and especially the vestibular system that functions even in the absence of vision—directly guide these motor actions. Indeed, in other tasks focused, for example, on the control of body configurations, compensatory reactions can be primarily based on proprioceptive feedback, as seems to be the case during postural regulation in rabbits (Beloozerova et al. 2003a,b; Deliagina et al. 2000).
Adaptation of the vestibulospinal system
In the long term, in UVL patients, vestibular symptoms fade away after compensation provided by the intact side of the vestibular system and as the result of learning and adaptation usually occurring when visual cues are available (Borel et al. 2002). Unlike healthy subjects and despite the compensations that occurred after the surgery, most UVL patients in our study manifested impairments in making appropriate adjustments to preserve motor actions in external space during changing trunk conditions. Our results, as well as results of clinical testing (Tables 1–3), show that substantial motor deficits in UVL patients persist well beyond the recovery period of 6 mo defined by Maurer et al. (2002).
When required to maintain the same hand position, patients 1 and 2 were unable to appropriately modify arm joint angles, so that the changes in the hand position almost mirrored the trunk motion, reflected in low compensation gains. These patients thus maintained the hand position in a body-centered reference frame, whereas the task required maintaining it in the external frame of reference linked to the environment. Ghafouri and Feldman (2001) showed that healthy subjects can rapidly perform similar arm movements in different frames of reference depending on the task requirements, such as when the target was on the body or in the external space. The present findings show that long after surgery, most UVL patients are unable to adjust the arm interjoint coordination to transfer motor actions from one spatial frame of reference to another.
Compared with patients 1 and 2, deficits in arm–trunk coordination in patients 3–6 were less severe. Regardless of the severity, compared with healthy subjects, when the trunk motion was blocked, hand trajectories in patients 1–6 began to diverge from the trajectories obtained in free-trunk trials, when the hand covered 50–65% of the movement distance. In these patients, a large part (40–70%) of the sagittal hand displacement was provided by the trunk movement (see RESULTS). Thus except for patient 7, all UVL patients had difficulties in transforming their arm actions performed within the body frame to those requiring reaching the goal in the external ("absolute") frame of reference. Patient 7 was a former airplane pilot. It is possible that skills developed before the vestibular loss, which include the ability to use vestibular signals to perceive and control the aircraft motion (Hosman et al. 1999) as well as a better sensitivity to proprioceptive signals, could have contributed to his higher level of compensation compared with that of the other UVL patients. This patient moved his hand slightly backward when the trunk was moving forward during the task of hand stabilization near the contralateral target. This may indicate that he was skillful enough to prepare appropriate compensatory responses in a feedforward way and trigger them at a short latency in respective trials. Similar adaptation from vestibular deficits in a pilot who guided aircrafts for 10 yr after UVL was previously reported by Kortschot and Oosterveld (1995).
The side of the vestibular lesion did not influence our main results. In addition, the target position (ipsi- or contralateral) did not influence the arm–trunk compensation gains. These data may be related to the ability of one side of the vestibular system to use bilateral projections to compensate for deficiencies resulting from a contralateral lesion during long-term adaptation (Beraneck et al. 2004; de Waele et al. 1990; Lacour et al. 1997; Straka et al. 2005; Vibert et al. 1999). However, compensation gains in patients were mostly lower than those in healthy subjects, showing that the descending bilateral projections from the intact side of the vestibular system cannot adequately compensate for deficits caused by the UVL, even after long periods of adaptation. According to clinical tests made a month before or after our experiments (Table 1), the patients showed no sign of dizziness, impairment in postural stability, or locomotion in the presence of vision. However, the scores on the tests that indirectly evaluate the VOR—the dynamic visual acuity test and Halmagyi impulse test—in these patients were low compared with those of healthy control subjects. These clinical data and our results imply that, despite long-term adaptation, motor deficits elicited by UVL are compensated by vision, whereas the restoration of the vestibular function remained incomplete. This also means that the vestibular system may not be considered as consisting of separate left and right sides: these sides function together, as a unit, possibly as the result of mutual interactions between them at the brain stem and other central levels so that one side cannot fully compensate for damage to the other side.
In conclusion, most UVL patients have deficits in the maintenance of a stable hand position or trajectory in the environment when trunk movement is involved. This implies that, in healthy subjects, the vestibular system provides equivalent motor actions regardless of the number of body segments involved in the task. Of the two tasks we studied, the hand stabilization task seemed to be more discriminatory in detecting the persistent impairment in arm–trunk compensatory coordination. Additional experiments are necessary before this task may be suggested as a diagnostic test of vestibulospinal deficiency in the ability to accomplish motor equivalent actions.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: A. G. Feldman, Center for Multidisciplinary Research in Rehabilitation, Rehabilitation Institute of Montreal, Quebec, Canada H3S 2J4 (E-mail: feldman{at}med.umontreal.ca)
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INTRODUCTION
