Brain, Vol. 125, No. 4, 880-894,
April 2002
© 2002 Guarantors of Brain
Deficits and recovery of head and trunk orientation and stabilization after unilateral vestibular loss
1 Laboratoire de Neurobiologie Intégrative et Adaptative, Université de Provence/CNRS and 2 Service ORL et Chirurgie cervico-faciale, Hôpital Nord, Marseille, France
Correspondence to: Liliane Borel, Laboratoire de Neurobiologie Intégrative et Adaptative, Université de Provence/CNRS Centre de St Jérôme, F-13397 Marseille Cedex 20, France E-mail: boul{at}up.univ-mrs.fr
Received April 30, 2001. Revised December 31, 2001. Accepted November 8, 2001.
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Summary |
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The aim of the study was to analyse changes in the orientation and stabilization of the head and trunk and their recovery after complete unilateral loss of vestibular information in humans. The ability of nine Ménière’s patients to orient and stabilize their heads and trunks in space was investigated during a simple dynamic task of knee-bends and compared with the performance of 10 healthy subjects. Patients’ performance was recorded before unilateral vestibular neurotomy (UVN) and during the time-course of recovery (1 week, 1 month, 3 months). Experiments were performed both in eyes open (EO) and eyes closed (EC) conditions to evaluate the role of visual cues in the recovery process. Head and trunk mean angular position (orientation) and mean maximal angular rotation (stabilization) in the roll plane and the yaw plane were recorded using a video motion analysis system. The results indicate that, in the acute stage after UVN (1 week), patients exhibit marked impairments in head and trunk orientation in both visual conditions. In the EC condition, head and trunk were deviated towards the operated side in the roll plane and the yaw plane. Head and trunk stabilization in space was impaired in the roll plane and associated with increased stabilization of the head on the shoulders. Interestingly, vision caused a complete inversion of the orientation pattern, with head and trunk rotations towards the intact side in the roll plane and the yaw plane. Relative to darkness, vision also reduced head and trunk oscillations. Recovery from abnormal head orientation in the light and impaired head stability in both visual conditions was achieved within 1 month and 3 months after UVN, respectively. However, head and trunk orientation in the dark and trunk stabilization in the roll plane remained uncompensated 3 months post-lesion. These results suggest that unilateral vestibular loss leads to a postural syndrome similar to that described previously for various animal species. They confirm the necessity of vestibular inputs for properly stabilizing head and trunk during self-generated displacements in healthy subjects. They also support the notion that vestibular compensation relies on visual cues whose substitution role gradually decreases after UVN.
Keywords: head and trunk postural control; unilateral vestibular neurotomy; recovery time-course; visual substitution; human
Abbreviations: AI= anchoring index; CCF = cross correlation function; D–1 = tests carried out before surgery; D+7 = tests carried out 1 week after surgery; D+30 = tests carried out 1 month after surgery; D+90 = tests carried out 3 months after surgery; EC = eyes closed; EO = eyes open; UVN = unilateral vestibular neurotomy
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Introduction |
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Postural balance control is a highly integrative process based on the interaction of different sensory modalities, among which vestibular and visual cues take a prominent part. Postural control requires that head stabilization and head orientation be preserved in space. Studies performed with healthy subjects have demonstrated head stabilization and orientation in space with a precision of a few degrees during natural dynamic activities. Spatial head stability has been described for the sagittal plane during locomotion (Berthoz and Pozzo, 1988
; Pozzo et al., 1990) and for the yaw plane during complex equilibrium tasks (Mouchnino et al., 1992; Pozzo et al., 1995). Head stabilization, though incomplete, plays a large role in gaze stabilization since the remaining head oscillations are compensated for by the vestibulo-ocular reflex (Grossman et al., 1988, 1989).
Unilateral loss of the vestibular inputs induces a typical postural syndrome including head postural deficits, body torsion about the longitudinal axis and decreased tone in the limbs ipsilateral to the injured side. The unilateral ataxia resulting from vestibular lesion has been studied extensively in various animal species (cf. Lacour and Borel, 1993; Dieringer, 1995). For humans, Nelson (1968) and Fregly (1974) produced evidence for the functional importance of vestibular sensors for posture and equilibrium by using an ataxia test battery. They showed that patients with unilateral vestibular loss suffered from disequilibrium and tended to fall to the side ipsilateral to the lesion. Dynamic posturography methods as well as motion analysis systems now provide the means for thorough investigations of the ability of vestibular defective patients to stabilize various body segments in space. How patients with impaired vestibular function stabilize their heads in space is a topic of interest that has been studied mostly in patients with bilateral vestibular loss. Oscillations of the head are increased in the yaw plane during passive and unpredictable body rotations (Guitton et al., 1986; Gresty, 1987; Bronstein, 1988) and in the vertical plane during walking, running or hopping (Grossman and Leigh, 1990; Takahashi, 1990; Pozzo et al., 1991). These data are corroborated by experiments performed immediately after space flight that showed decreased head stabilization (Reschke et al., 1994). The effect of unilateral labyrinthine dysfunction on spatial head stability is still debated; few studies have reported a reduced control of head stabilization in such patients (Taguchi et al., 1984; Takahashi et al., 1988). No studies, however, have investigated head and trunk orientation and stabilization after acute vestibular unilateral deficits and their subsequent recovery in humans.
In the present experiment, we asked whether complete unilateral loss of vestibular information in humans impairs orientation and stabilization of the head and trunk. To answer this question, we investigated the postural control of Ménière’s patients who underwent a unilateral vestibular neurotomy (UVN) as surgical treatment for the incapacitating forms of peripheral vertigo encountered in this disease. This investigation was performed during a simple dynamic task consisting of repeated knee-bends.
Another main issue was the substitution role of visual cues in the compensation of head and trunk orientation and stabilization. Vision was manipulated through eyes open (EO) and eyes closed (EC) conditions. To determine the recovery time-course of the functional deficits and the underlying mechanisms for recovery of postural control over time, we examined patients at three postoperative times: 1 week (D+7); 1 month (D+30); and 3 months (D+90). Head and trunk kinematics were investigated by a motion analysis system. Our work focuses on the analysis of head and trunk angular position (orientation) and their maximal angular rotation (stabilization) in the roll plane and the yaw plane. The ability of patients to preserve head and trunk balance was compared with that of healthy control subjects.
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Methods |
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Subjects
Data from nine patients suffering from unilateral Ménière’s disease (four females and five males, aged between 28 and 63 years, mean age 45 years) were compared with those from 10 healthy volunteers (five females, five males, aged between 22 and 56 years, mean age 40 years). Each of them gave informed consent to the study, which was approved by the local ethics committee (CCPPRB Aix-Marseille I). All the patients complained about hearing loss, tinnitus and frequent uncontrolled attacks of vertigo leading to gradual disablement. Vestibular and auditory tests established that all the patients exhibited pure unilateral deficits. Hearing loss averaged 52% (range 10–85%) and vestibular dysfunction determined by the caloric test averaged 52% (range 20–100%). On average, patients suffered their first attack of vertigo 10 years ago (range 2–15 years). Patients with additional motor or visuomotor disorders were excluded from the study. After a clear failure of medical therapy for patients who became pharmacology-resistant, neurotomy was used to eliminate vertigo and to preserve hearing. The surgical procedure was a retrosigmoid vestibular nerve section (see Magnan et al., 1990
, 1991). Of the nine patients, six had a right-side lesion and three a left-side lesion. The patients were tested four times: the first test was carried out before surgery (D–1) in the latent phase of the disease, i.e. when they had not exhibited attacks of vertigo during the preceding week. The other tests were carried out postoperatively during the acute stage (D+7) and the compensatory stage (D+30 and D+90). Since familiarity with the task might have modified their responses, a group of five control subjects was tested at the same time intervals. Because we verified that responses were stable over time in those subjects (see Fig. 3), a single test was performed for the control population.
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Experimental procedures
The subjects were asked to perform knee-bends. This simple dynamic task was used to test the patients’ ability to dynamically preserve balance in a natural condition. The subjects were told to use their own frequency and amplitude of flexion in order to test head and body orientation and stabilization in a range of natural movements. They performed eight consecutive knee-bend cycles barefooted during each trial; a cycle included one flexion and one extension (see Figs 1 and 2). The ability of the patients and healthy subjects to stabilize and orient their heads and bodies in space was tested both in light (EO) and in darkness (EC). In the light, the subjects were required to perform the movement while looking at a target 6 m in front of them. In darkness, the subjects were instructed to stabilize their gaze on the memorized target while performing the task; occluding goggles were placed on the subject’s head to suppress cues from remaining brightness that could give information about changes of head and body position in space.
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Data acquisition
Kinematic analysis was performed with a video motion analyser (ELITE system, BTS, Milan, Italy). Two cameras were positioned 4.5 m in front of the subject. The infrared video cameras (BTS, Milan, Italy) recognized infrared reflecting markers (8 mm in diameter). Fourteen markers were placed full face on the head, chin, sternal fork, acromions, iliac crests, patellas, ankles and distal phalanx of the big toes. The markers defined a morphological model (stick diagram) that gave the position of the whole body in space (see Figs. 1A and 2A) and allowed us to compute orientation and stabilization in the roll and yaw planes.
Data processing
Marker positions were sampled every 10 ms (100 Hz). The ELITE system detects markers through shape recognition and computes marker centroid coordinates for both cameras. Calibration was carried out before the experiments and a consistent model was created. The ELITE system elaborated marker trajectories and 3D reconstruction (cf. Ferrigno and Pedotti, 1985) on the basis of these parameters. In our experimental set-up, the overall accuracy of marker angular position was 
0.02°.
The orientation was defined as mean angular position of the head and trunk with respect to gravitational vertical and to the horizontal. Head orientation in the roll plane and yaw plane was defined by the infra-orbital line with respect to the vertical axis and the horizontal (left–right) axis, respectively. Shoulder and hip orientation were recorded separately and jointly processed as trunk orientation. Trunk orientation in the roll plane and yaw plane was assessed by computing the position of the medial line from half-distance between the markers on the acromions to half-distance between the markers on the iliac crests, with respect to the vertical axis and the horizontal axis. We proceeded in such a way for two reasons: first, similar values were obtained when we compared shoulder and hip orientation in the roll plane and yaw plane; secondly, postural deviations were represented more directly by the position of the trunk than that of the shoulders and hips independently. A 0° angle indicates a lack of deviation with respect to the vertical or horizontal axes. Positive and negative signs refer to deviations towards the intact and operated sides, respectively, for the patients, and deviations towards the left and the right, respectively, for the controls.
The stabilization was expressed as the mean maximal angular rotation of individual body segments. Head, shoulder and hip stabilization were assessed in the roll plane and yaw plane. The more maximal angular rotation was reduced, the more segment stabilization was improved. Maximal angular displacement was averaged for each eight consecutive cycles of a single trial. Trials in which subjects fell were excluded from data analysis.
The data processing described above concerns the orientation and stabilization of the different segments in space. To determine how the head was stabilized on the shoulders, i.e. to know if head and trunk posture rely on dependent or independent mechanisms, we completed the kinematic approach by computing an anchoring index (AI) (cf. Amblard et al., 1997) and a cross correlation function (CCF) (cf. Amblard et al., 1994; Lekhel et al., 1994).
The AI aimed to compare the stabilization of the head with respect to the shoulder and to space. The AI was expressed as follows:
AI = (
2r – 2a)/(2r + 2a)
where 2a is the absolute angular deviation and 2r is the relative angular deviation. Positive and negative values of AI indicate that the head is preferentially stabilized in space and on the shoulders, respectively.
The CCF was assumed to extract the temporal relationship between head and shoulder movements. Average CCFs were calculated for each subject and expressed by the CCF coefficient peaks. Maximum positive CCF coefficients correspond to coordinated movements of the head and shoulders in the same direction, whereas minimum negative CCF coefficients correspond to head and shoulder variations in opposite directions.
Since both the AI and the CCF coefficient are in the range –1 to +1, we used a z transform to convert the values to an unbiased Gaussian distribution. Statistical analysis was performed on these normalized values.
Figures 1 and 2 show a general image of the whole body posture during knee-bends (using stick figures) and raw trajectories from a typical healthy subject and a typical patient, respectively.
Each dependent variable described above was analysed using a four-way (subjects x visual condition x flexion–extension x cycles) ANOVA (analysis of variance). Supplementary ANOVAs were performed for the Ménière’s patients to test post-lesion changes in both visual conditions. Tukey’s honestly significant difference (HSD) test (see Howell, 1994) was used as a post hoc test. Differences were considered statistically significant if P < 0.05.
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Dynamic content of the task
Table 1 shows task frequency and vertical maximum velocity during flexions and extensions for the patients at different postoperative times and for the controls. The mean frequency of the subjects’ vertical displacement during the knee-bend task (calculated from the marker placed on the sternum) and mean vertical maximum velocity (Vmax) during both flexions and extensions were similar for controls and patients whatever the postoperative time (D–1, D+7, D+30, D+90) and the visual condition (EC/EO).
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Fourier analysis of the head angular rotation showed a fundamental frequency ranging from 0.05 to 0.25 Hz in the roll plane and from 0.05 to 0.25 Hz in the yaw plane for both patients and controls. The peaks of the amplitude spectra differed strongly from the mean frequency of the subjects’ vertical displacement during the knee-bend task (0.5–0.75 Hz).
The CCF showed an interaction between the subjects’ vertical displacement and the head angular rotation in the roll plane, with a phase relationship between the signals. However, the correlation peak was either positive or negative and varied from 0.3 to 0.8 depending on the subjects. In addition, for an individual subject, the relationship varied between sessions: it could be present or not and positive or negative irrespective of the postoperative time and the visual condition. In the yaw plane, the head angular rotation was generally not correlated to the subjects’ vertical displacement and, when present, the correlation peaks were below those in the roll plane. Finally, the correlation in the yaw plane was not associated with the correlation in the roll plane.
Consequently, we found no clear relationship between the subjects’ vertical displacement and the head angular rotation in either the roll plane or the yaw plane. If a relationship was present, it was found not to be part of the dynamic content of the task. Furthermore, a relationship was rare and irrespective of the subject (patients or healthy subjects), the postoperative time (D–1, D+7, D+30, D+90) and the visual condition (EC/EO). Consequently, the dynamic content of the task was discarded in subsequent analyses and the focus placed on the head angular position (head orientation) and maximal head angular rotation (head stabilization).
We first studied these parameters separately over each of the eight consecutive cycles of a single trial for the flexions and the extensions. Figure 3 illustrates the data recorded in the roll plane for one patient and one control subject in EC and EO conditions through the four recording sessions. For the patient, the head orientation changed after UVN both in EC and EO conditions. In contrast, for the control, the head angular position was stable over time. ANOVA on the whole population indicated that head orientation did not differ significantly within the same experimental session, neither over cycles (F = 0.95; P < 0.46), nor during the flexion and extension phases (F = 0.02; P < 0.88). Thus, we decided to present mean data for averaged cycles and by pooling the flexions and the extensions.
Orientation in the roll plane
The ANOVA indicated that subjects (F = 6.7; P < 0.0001) and visual conditions (F = 183.5; P < 0.0001) constituted the main effects for the variations of mean head angular position. Post hoc Tukey’s HSD test revealed that the mean head angular position was tilted in the roll plane for patients tested in the acute stage after the lesion (Fig. 4). In darkness, the head was significantly tilted towards the lesioned side (P < 0.0001). Interestingly, in the presence of visual cues, an opposite pattern of head position was seen, with a head tilt towards the intact side (P < 0.0001). In the EO condition, head orientation was restored within 1 month after surgical treatment. In the EC condition, the mean head orientation still differed from that of healthy subjects until the end of the third postoperative month (P < 0.05). In the light as well as in darkness, the mean head angular position did not differ between patients tested before surgery and the controls.
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As shown in Fig. 4, the mean trunk angular position revealed similar directions of tilt in the roll plane just after UVN, with a deviation towards the operated and the intact side in EC (P < 0.05) and EO (P < 0.0001) conditions, respectively.
Orientation in the yaw plane
An overall significant effect of subjects (F = 25.4; P < 0.0001) and visual condition (F = 194.9; P < 0.0001) was also found in the yaw plane. Detailed analyses revealed the impairment of the head angular position became obvious in the acute stage after neurotomy, with head deviation towards the operated side (P < 0.0001) in the EC condition and towards the intact side (P < 0.0001) in the EO condition (Fig. 5). Recovery of the head angular position in the yaw plane was observed the first postoperative month in the light, while recovery was not achieved after 3 months in darkness. When tested before UVN, patients behaved like healthy subjects.
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Trunk orientation changes were close to those of the head. Trunk was rotated towards the operated side in darkness from D+7 to D+90. Rotation towards the intact side in the light was recorded in the acute stage only after UVN.
From the first to the last cycle of the task, i.e. from cycle 1 to cycle 8, a drift was noticed for both the head and trunk angular position in the yaw plane. ANOVA on the head and trunk angular position showed a significant effect of cycles (F = 4.3; P < 0.0001 for the head and F = 35.6; P < 0.0001 for the trunk angular position). Figure 6A shows the mean head angular position calculated for each cycle for patients in the acute stage after UVN and the controls under EC and EO conditions. Progressive deviations appeared for patients, while mean values stayed close to zero for controls. To characterize the progressive deviation, we calculated the mean slope of head angular position from the first to the eighth cycle (Fig. 6B). For the patients, the results indicated a progressive deviation towards the operated side in EC conditions, whatever the test time (D–1, P = 0.05; D+7, P = 0.005; D+30, P < 0.05; D+90, P < 0.001) and towards the intact side in EO conditions only during the acute stage (D+7, P < 0.01).
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Stabilization in the roll plane
The mean head, shoulder and hip maximal angular rotations increased in patients (Fig. 7). One week after UVN and in darkness, the increase averaged 200% (P < 0.0001), 215% (P < 0.0001) and 180% (P < 0.0001) with respect to control data for the head, shoulders and hips, respectively. Data recorded in the light showed smaller but significant modifications (130%, P < 0.05 for the head; 160%; P < 0.0001 for the shoulders; and 156%; P < 0.0001 for the hips). Taken together, these results point to impaired head, shoulder and hip stabilization. In the third postoperative month, maximal head angular rotation values were similar to those of the controls both in EO and EC conditions. However, shoulder and hip maximal angular rotation compared with the controls was still increased 3 months after surgery whatever the visual condition. This means that shoulder and hip stabilization remained impaired at this late stage. Maximal angular rotations were also higher in patients before UVN [the average increase in head angular rotation was 138% (P < 0.001) in the light and 139% (P < 0.05) in darkness].
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To determine whether head and trunk posture rely on dependent or independent mechanisms, we computed the AI and CCF between the head and shoulders. Figure 8A compares the mean AI for patients and controls in both EO and EC conditions. The ANOVA indicated that the AI differed significantly between patients and controls (F = 6.5; P < 0.001). Typically, in the EC condition, the AI significantly decreased after UVN at D+7 (P < 0.001) and D+30 (P < 0.001), indicating that the head was better stabilized on the shoulders than in space. At the third postoperative month, mean AI values did not differ from those of the controls. In the EO condition, AI was significantly decreased in the acute stage only after UVN (D+7, P < 0.05).
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Concomitant changes were observed for the CCF coefficient (Fig. 8B). Correlation coefficients increased and reached maximum values at D+7 (P < 0.0001) and D+30 (P < 0.001) in darkness, and at D+7 only (P < 0.001) in the light. The data indicate coordinated movements of the head and shoulders in the same direction after UVN.
Stabilization in the yaw plane
Figure 9 illustrates the mean maximal angular rotation for the head, shoulders and hips in the yaw plane. For controls as for patients, the mean angular rotations were higher in the yaw plane than in the roll plane. Mean maximal head angular rotations were three to four times as high as those recorded in the roll plane. In addition, in the acute stage after UVN, planned comparisons show that, in the light, the maximum head angular rotation was significantly reduced with respect to the control values (85%; P = 0.01). Shoulder and hip maximal angular rotation remained similar in patients and healthy subjects, whatever the recording session and the visual condition.
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Discussion |
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This study investigated the ability of total unilateral vestibular defective subjects (neurotomized Ménière’s patients) to orient and stabilize their heads and trunks in space during a natural dynamic task of knee-bends in EO and EC conditions. Patients’ performance was analysed before and after a UVN at different postoperative times and compared with that of a control population of healthy subjects.
Effects of vestibular lesion on head and trunk orientation
Head and trunk orientations in the roll plane and yaw plane are impaired after UVN. Evidence of impaired orientation is that, in the EC condition, the patient’s head and trunk deviated both in the roll plane and the yaw plane towards the operated side while healthy subjects kept a symmetrical posture. We found that these deviations depended on the visual condition, since patients presented an opposite pattern of postural disturbances in the EO condition, with head and trunk deviations towards the intact side in the roll plane and the yaw plane. The head and (or) trunk postural deviations in the EC condition in the yaw plane as well as in the roll plane showed that >3 months are necessary for central compensation, while orientation recovery was achieved within 1 month in the EO condition.
The modifications of head orientation in the EC condition we found for humans correlates with the results reported for various animal species (for a review, see Curthoys and Halmagyi, 1995). Specifically, head postural deficits consist of deviations in both the roll and yaw planes. In humans, a medical case with a dramatic 10° head tilt in the roll plane was reported by Halmagyi et al. (1979) for one patient after a unilateral labyrinthine lesion. The kind of lesion (vestibular neurotomy versus damage of the utricular macula or utricular nerve) could account for these discrepancies. Although such a large deviation was not observed in this study, head deviation was observed in both planes for all patients. In fact, the small amplitude of deviation could be why head deviations in both the roll plane and yaw plane had been poorly documented in humans. The use of a highly precise system of motion detection (system ELITE) could account for these observations.
The modifications of trunk orientation towards the operated side in the EC condition correspond to those reported for lesion-induced modifications in the vestibulospinal influences resulting from the unilateral vestibular lesion. Tone asymmetries in leg muscles have been described in animal models (Igarashi et al., 1972; Lacour et al., 1979) and in vestibular patients (Allum and Pfaltz, 1985). These studies all point to asymmetric EMG activity with the largest responses on the side contralateral to the unilateral deficit. Since our results point to asymmetrical postural responses, they can be taken as indirect evidence of the contribution of vestibulospinal inputs to the postural control of the head and trunk during self-generated displacements in healthy subjects. The AI and CCF coefficient calculated after UVN in the roll plane indicate that the head and shoulders were coordinated and that the head was stabilized on the shoulders. The data suggest, therefore, that head and trunk posture rely on dependent mechanisms—a hypothesis supporting the vestibulospinal contribution to postural control. An alternative explanation for the results could be that subjects with unilateral loss have an asymmetrical internal representation of the vertical about which they are actively reorienting their head and trunk. The progressively impaired head and trunk orientation in the yaw plane in the EC condition during the eight consecutive knee-bend cycles could bear witness to such a progressive reorientation of the head and trunk.
To our knowledge, the opposite pattern of head and trunk postural disturbances reported here for the EO condition has never been described. The short period during which they were observed (they disappeared 1 month after UVN) could account for this lack of description. Only Marchand et al. (1988) has drawn attention to a decrease in head tilt in kittens, which sometimes even overshot the vertical when vision was available. The literature dealing with the role of vision in the recovery process shows species-dependent effects. In humans, the weight of visual cues may be so sharply enhanced that vision could enable the inversion of postural asymmetries. At first glance, these results could account for over-compensation processes. However, we have recently demonstrated that, for patients standing quietly, the reversal of the head position in the EO condition is related to the presence of visual vertical and horizontal coordinates providing external reference frames, and that postural reversal is related to perceptive modifications (Borel et al., 2001). We hypothesize, therefore, that the deviation of the head and trunk corresponds to a reorientation of the head and trunk to an altered subjective visual vertical. In line with this view, reversal of the postural position towards the intact side in the EO condition could result from an attempt to align the torted retinal meridia to the visual vertical coordinates, since after UVN both eyes roll upper pole to the operated side (Curthoys et al., 1991a). In support of this view is the observation that eye cyclotorsion after UVN remained unchanged in light and in darkness (Borel et al., 2001) and that it declined in a similar way in both conditions with the progressive decrease of head tilt in the roll plane.
Another interesting feature of this study is that the trunk and head deviated in the same direction during the knee-bends throughout the postoperative period. A compensatory behaviour would have led to a counter roll tilt of the head with respect to the trunk to maintain the head stable in space. The lack of such a compensatory response could be related either to the deterioration of the vestibular head righting reflexes described in animals in response to body tilt (Putkonen et al., 1977; Courjon and Jeannerod, 1979) or, as discussed below, to increased head stabilization on the shoulders.
Recovery of the head and trunk orientation in the EC condition is not totally achieved by the third month following neurotomy as patients still differ from controls in their ability to achieve postural symmetry in the yaw plane. Therefore, it appears either that periods longer than 3 months are needed for compensation of postural control or that head and trunk orientation changes are part of vestibular sub-processes which, in humans, constitute a permanent legacy of unilateral vestibular deafferentation like tonic ocular torsion (Curthoys et al., 1991a), tilt of the visual subjective vertical (Friedmann, 1971) and roll tilt perception (Halmagyi et al., 1993). Recovery of trunk orientation, however, is faster than that of the head in the roll plane. This could be explained by a stronger vestibular control on the head than on the trunk as the amount of direct vestibulospinal tracts are greater for the cervical than for the thoracic levels. The higher amount of surface somatosensory information for the trunk could also account for the difference in the time-course recovery of the head and trunk. Taken together, these data can be related to a top-down influence of the vestibular system versus a bottom-up control by the somatosensory information (Mergner et al., 1997).
Effects of vestibular lesion on head and trunk stabilization
In this study, we have shown that head and trunk stability in space was impaired in the frontal plane. Patients with an acute vestibular lesion exhibited greater maximal angular rotation of the head, shoulders and hips in the roll plane than healthy subjects in both visual conditions. In addition, they possessed increased head stabilization on the shoulders. Concomitantly, head stability in space was increased in the yaw plane acutely after UVN in the EO condition as angular deviations were smaller than those of the control subjects. We found that recovery of head stabilization was achieved 3 months after UVN, while shoulder and hip stabilization did not regain normal values—as evidenced by higher maximal angular rotations for patients in the roll plane than for controls both in EO and EC conditions.
That head and trunk stability in space is impaired after UVN in the roll plane is in partial agreement with the studies of Taguchi et al. (1984) and Takahashi et al. (1988) dealing with the effect of unilateral labyrinthine dysfunction on spatial head stability. Taguchi et al. (1984) showed greater head instability in all three spatial planes of space during stepping, while Takahashi et al. (1988) found increased right–left and forward–backward oscillations of the head only during running. These differences could also be accounted for by the kind of lesion (fluctuating vestibular loss versus total unilateral loss of vestibular afferences). Taken together, the results suggest that head stability depends on the motor task. In addition, our results indicate that healthy subjects stabilized their heads and trunks accurately. These results are consistent with previous reports indicating an efficient stabilization of the head in space during locomotion and during various complex dynamic equilibrium tasks (Grossman et al., 1988; Pozzo et al., 1990, 1995). The overall data confirm that the vestibular system provides inputs necessary to stabilize the head and trunk during self-generated displacements in healthy subjects. In the acute stage after the lesion, vision reduced head and trunk angular displacement compared with those recorded in darkness, corroborating the general statement that vestibular compensation relies strongly on visual cues.
Interestingly, the impaired head stabilization in space in the roll plane is associated with an increased head stabilization on the shoulders and with coordinated movements of the head and shoulders. The results indicate that such changes in kinematics parameters are found up to 1 month after UVN in the EC condition and in the acute stage (D+7) only in the EO condition. They argue for dependent mechanisms for head and trunk postural control. With regard to the control subjects, the knee-bend task did not promote better stabilization of the head in space or on the shoulders. Another major result was that head stabilization in space was not impaired in the yaw plane. In constrast, in the acute stage after UVN, patients succeeded better in stabilizing their head in space in EO condition than did control subjects. We suggest that these results proceed from the increased stabilization of the head on the trunk described previously in the roll plane. Considering the whole of the data described above, we hypothesize that both the increased head stabilization on the shoulders in the roll plane and the reduced head oscillations in space in the yaw plane account for the increased stiffness of the head on the trunk. Increasing ankle stiffness in the presence of vision has recently been demonstrated in healthy participants when balance confidence was compromised (Carpenter et al., 1999). Although the present experiments did not produce the data necessary to test the assumption of an increased stiffness of the head on the trunk, strategies reducing head on trunk motion have been found in vestibular patients with bilateral (Dichgans and Diener, 1989; Maurer et al., 1998) or unilateral compensated (Katsarkas and Segal, 1988) loss after exposure to rapid head turns. Such a reduction in head angular oscillation, especially in the lateral plane (referred to as head on trunk blocking) has been also reported in patients with Parkinson’s disease (Mesure et al., 1999). Finally, we found increased stiffening of the head on the trunk in cats submitted to vertical linear displacements after UVN (Gustave Dit Duflo et al., 1998). Functionally, increased stiffening restricts vestibular stimulation and, subsequently, optimizes gaze stabilization during the subject’s displacement. Moreover, since this strategy is also known to be involved in the ontogenesis of head stabilization (Assaiante and Amblard, 1993), it could therefore constitute a return to a strategy used before the head stabilization sensorimotor systems are fully matured.
Following neurotomy, head stabilization is regained at a basically normal level 3 months after UVN in the roll plane with mean values of head angular rotation in space, AI and CCF coefficient similar to those of the controls. However, shoulder and hip stabilization is not totally recovered. These results fit with the top-down approach of postural control described by Berthoz and Pozzo (1988). In other respects, they suggest that the remaining labyrinth is insufficient to keep perfect postural control even 3 months after UVN. Our data agree with those of Allum et al. (1988), who showed that vestibulospinal reflex compensation required considerably longer than 2 months for unilateral patients. Three months after UVN, head and trunk stabilization changes were similar in both visual conditions, suggesting that visual substitution processes decreased gradually after unilateral vestibular deafferentation. Indeed, a transitory substitution role of visual cues, limited to the first three post-lesion weeks, has been reported in behavioural and electrophysiological studies in UVN monkeys and cats (Lacour et al., 1981; Zennou-Azogui et al., 1996).
Finally, the present data indicate that the patient’s preoperative status differs from that of the healthy subject. Evidence of impaired postural control is that the maximal angular rotations of the head, shoulder and hip were increased in both EO and EC conditions. However, preoperative orientation of the patients’ head and trunk did not differ from those of the controls. None of the patients had near normal caloric responses preoperatively, but exhibited small caloric responses on the affected side. Therefore, their partial vestibular loss may have not been fully compensated. This result could have implications for its use in diagnosis.
In summary, we have shown that unilateral loss of vestibular function in humans causes an impairment of postural control similar to that described for animal species since, in the EC condition, the head and trunk are deviated towards the operated side both in the roll plane and the yaw plane. The underlying mechanism for recovery of postural control includes: (i) a powerful impact of vision allowing postural deviations to be reversed in the acute stage after vestibular loss; (ii) an increased head stabilization on the trunk in the acute stage after UVN and more extended in time when visual cues are lacking; (iii) a transitory substitution role of visual cues gradually decreasing over time; and (iv) a lack of total compensation by the remaining labyrinth as evidenced by the remaining head and trunk orientation and stabilization deficits 3 months after UVN.
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We thank Bernard Amblard for help in the kinematics approach for the anchoring index. This study was supported by grants from CNRS and Ministère de l’Enseignement Supérieur et de la Recherche (UMR 6562 CNRS/Université de Provence).
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