Static and Dynamic Balance Function in Spasmodic Torticollis

Transcription

1 Movement Disorders Vol. 14, No. 1, 1999, pp Movement Disorder Society Static and Dynamic Balance Function in Spasmodic Torticollis *Marion Simonetta Moreau, MD, PhD, Alexandra Séverac Cauquil, PhD, and *Marie Claude Costes Salon, MD *Service d Exploration Fonctionnelle Sensorielle et Motrice, Toulouse, France; and Centre de recherche Cerveau et Cognition UMR 5549, Toulouse, France Summary: The consequences of abnormal head posture on static and dynamic balance skill were studied in a group of 10 patients with idiopathic spasmodic torticollis (ST). In static conditions, body sway was assessed using a conventional force platform with eyes open and with eyes closed. Standardized dynamic balance conditions were produced using a rocking platform; lateral and anteroposterior dynamic balance skills were assessed by measuring linear displacement both of the body base and of the head. Dynamic tests were repeated 6 weeks after botulinum toxin treatment in all patients. Patients results were compared with those obtained from 10 control subjects. In static conditions, ST patients did not differ from control subjects, but in dynamic conditions, balance parameters were greater in the patient group than in the control group. This was true for the lateral direction and for dynamic balance parameters recorded both before and after botulinum toxin treatment. Eye closure significantly increased dynamic balance parameters in both groups. However, the effect of eye closure was greater in the patient group than the control group, especially for lateral sway, suggesting that patients used vision to compensate for the dynamic balance disturbance induced by the spasmodic torticollis. Despite a significant improvement of head posture in all patients after botulinum toxin treatment, no significant changes in dynamic balance parameters were observed between the first and second test. The possible origins of the dynamic balance disturbance observed in ST patients are discussed. Key Words: Balance Spasmodic torticollis Posturography. Received October 23, 1997; revision received March 6, Accepted May 18, Address correspondence and reprint requests to Marion Simonetta Moreau, MD, PhD, Laboratoire de Physiologie, 133 route de Narbonne 31062, Toulouse, France. Spasmodic torticollis (ST) is the most common form of focal dystonia. It is characterized by involuntary contraction of the neck muscles which results in tonic or clonic head movements and more or less sustained abnormal head posture. It is not known whether such abnormalities of the motor tone of the neck muscles will elicit balance disturbances. However, the neck, supporting the head and thus the sensory cephalic organs, allows, by its mobility, a spatial orientation which contributes to body stability. Through its motor function, it also plays an important role in the regulation of tonic muscular activity and thus postural stability. The consequences of abnormal head posture on static and dynamic balance were studied here, using a posturographic method, in a group of 10 patients with idiopathic spasmodic torticollis and a group of 10 age-matched control subjects. Static balance was assessed by measuring body sway, with eyes open and with eyes closed, on a conventional force platform. Dynamic balance was assessed using a rocking platform with a sensitive recording device, 1 under standardized conditions, with eyes open and with eyes closed. The effect of botulinum toxin treatment on dynamic balance performance was also studied in the group of patients with spasmodic torticollis to determine whether head posture improvement induced by the treatment was accompanied by an improvement in balance. MATERIALS AND METHODS Ten patients with isolated idiopathic ST (five men and five women; mean age 50 yrs, range yrs) participated in this study. All patients gave their informed consent to the experimental procedures, which had been approved by the local ethics committee. Only patients with a predominant involuntary horizontal fixed head rotation to the left (eight patients) or to the right (two patients) were included. Patients with additional head tremor, myoclonic head movements, or additional trunk or limb dystonia were excluded from the study. Mean disease duration was 3 years (range 1 10 yrs). Apart from the dystonic posture, neurologic examination was normal. Romberg s test was normal and there was no spontane- 87

2 88 M. S. MOREAU ET AL. ous nystagmus either in the primary position or with gaze deviated. Five of the patients had never been previously treated with botulinum toxin. The other five performed the first balance tests a minimum of 4 months after their last botulinum toxin injection. Other medications were continued as long as they had not been prescribed for the first time within a 2-month period before the beginning of the study. All patients performed a second dynamic balance test 6 weeks after botulinum toxin treatment. Mean dose of intramuscular Dysport botulinum toxin injection was 600 U ± 140 distributed among sternocleidomastoid, splenius capitis, and sometimes trapezius muscles. Clinical improvement of head posture after botulinum toxin injection was assessed by a simplified clinical score derived from the Toronto Western Spasmodic Torticollis Rating Scale 2 (Table 1). Scores were calculated before and 6 weeks after botulinum toxin treatment. Static balance was assessed using a conventional three-strain gauge force platform (width 46 cm, depth 46 cm, height 7.5 cm, weight 19 kg; QFP system approved by the French Association of Posturology). Center of pressure (CoP) displacement of the subject s foot was measured with a sampling frequency of 40 Hz. A microcomputer calculated the length (mm) and area (mm 2 )of the statokinesigram, mean lateral (x) and anteroposterior (y) position, and the length versus area coefficient. For these measurements, results obtained in patients were compared with the French Association of Posturology s standardized norms. 3 The linear component of head movement was measured using a device derived from Wright s ataxiameter. 4 A string was attached to the subject s head and then pulled taut over a pulley by a 20-g small weight. An optical coder was mounted on the pulley and was linked to a microcomputer; it sampled head displacements with a frequency of 100 Hz and an accuracy of 0.2 mm. Because this device measured only linear and not angular displacements of the head, its output should be regarded as a coarse global measure of head displacement in each condition. Dynamic balance conditions were obtained by having the subjects stand on an unstable rocking platform, 1 which was derived from a Freeman platform of the type used to develop coordination of the calf muscles. 5 The device consisted of a square platform (width 60 cm, depth 60 cm, height 6 cm [when horizontal], weight 2 kg) supported by a segment of a cylinder (radius 55 cm) which was in contact with the ground (Fig. 1B). The fixed characteristics of the platform produce standardized conditions for subject instability. The device reduces the support of a subject standing on it to a 60-cm line called the pivot, that is, the portion of the cylinder that is in contact with the ground. Linear displacement of the pivot on the ground was computed from the rotation of a lever, one extremity of which laid freely and slid with minimal friction on the ground according to the tilts of the platform. Lever rotation was assessed by an optical coder linked to a microcomputer which had a sampling frequency of 100 Hz and an accuracy of 0.7 mm. Head displacement was measured in the same plane as the pivot movements using the same method as in static conditions (Fig. 1A). Lateral and anteroposterior sway were assessed separately according to the subject s position on the platform. Lateral sway was measured with the subject standing along the pivot line (that is, parallel to it) and anteroposterior sway was measured with the subject standing at right angles to the pivot line (Fig. 1). Stance width was kept constant (feet 5 cm apart) regardless of the direction of sway. Dynamic balance skill was assessed by measuring si- TABLE 1. Clinical rating scale 1. Amplitude of sustained head movements (maximal excursion) Rotation: 0 absent, 1 <30, , , 4 > 60 Laterocollis: 0 absent, 1 <15, , 3 >30 Ante/Retrocollis: 0 absent, 1 mild, 2 moderate, 3 severe 2. Shoulder elevation/anterior displacement 0 absent, 1 mild and intermittent 2 mild and constant, or severe and intermittent 3 severe and constant 3. Duration of sustained movements 1 intermittent 2 constant 4. Range of motion 0 Able to move to extreme opposite position 1 Able to move head well past midline but not to extreme position 2 Able to move head barely past midline 3 Able to move head toward but not past midline 4 Barely able to move head beyond abnormal posture

3 BALANCE IN SPASMODIC TORTICOLLIS 89 FIG. 1. Materials and Methods: (A) The system used to measure head linear displacement; a string tightened between the headband fixed around the head and a pulley transmits head displacements to an optical coder (o.c.) fixed to the shaft of the pulley. (B) The device used to assess dynamic balance function; a platform with a curved base in contact with the ground through a line, the pivot. When the platform tilts, a lever fixed to an extremity of the platform slides on the ground and rotates around its point of fixation. The rotation is assessed by an optical coder (o.c.). Left: position of the subject on the platform to measure anteroposterior body sway; right: lateral body sway. multaneously the movement of both the pivot and the head. The microcomputer calculated the length of linear displacement of the pivot (PLD) and of the head (HLD), that is, the sum (in mm) of the absolute values of each displacement of the pivot and of the head. The PLD/HLD ratio provided a measure of the reduction of head movements with respect to pivot movements. Patients were compared with an age-matched group of 10 control subjects (mean age 48 yrs, range yrs). Experimental Protocol The subjects, who were wearing disposable slippers, were asked to stand first on the stable force platform for 50 sec with their eyes open followed by a 50-sec period with their eyes closed. During the eyes-open period, subjects fixated on an eye-level target on a wall approximately 3minfront of them. Then the subjects stood on the unstable platform and were asked to keep their balance, that is, to maintain the platform as horizontal as possible. A dynamic balance recording session, divided into two 25.6-sec periods (eyes open then eyes closed), started randomly either with lateral sway recording or with anteroposterior sway recording. During the eyes-open periods, subjects again fixated on an eye-level target on the wall. Patients performed a second dynamic balance task 6 weeks after botulinum toxin injection. For the control subjects, to assess the contribution of head position to balance skill, the test was performed not only with the head facing forward (HF condition) but also with it turned to the left and to the right (HL and HR conditions, respectively). HF, HL, and HR sequences were randomly alternated. Statistical Analysis Having assessed the normality of the distribution of our population using the Kolmogorov-Smirnov test, an analysis of variance (ANOVA) was used to compare the results between the different groups. First, a two-way repeated measures ANOVA was used to study the influence of spasmodic torticollis on dynamic balance parameters before botulinum toxin injection (ST1). The same comparison was then made between the control subjects data and the patients data collected after botulinum toxin treatment (ST2). The factors were the presence or absence of spasmodic torticollis (two levels: control group/st group) and the repeated measurements (two levels: eyes open/eyes closed). A further two-way repeated-measures ANOVA with two factors was performed in the ST group: treatment factor with two levels: before and after botulinum toxin, and vision factor with two levels: eyes open and eyes closed. A paired Student s t test was used to compare clinical scores before and after botulinum toxin treatment. In addition, a repeated-measures ANOVA with two factors was performed in the control group: head rotation factor with three levels: HF, HL, HR, and vision factor with two levels: eyes open and eyes closed. The same statistical method was used to compare the parameters obtained in the control group in HL conditions with the parameters obtained in the left ST subgroup (eight patients). For each statistical test, interac-

4 90 M. S. MOREAU ET AL. tions between the different factors were also investigated. For all statistical analyses an alpha level of 0.05 was used. Results were given as mean values ± standard deviation. RESULTS Static Balance Task For all but one patient, static body sway parameters were in the normal range. The exception showed an increase in body sway area and body sway length in eyes open and eyes closed conditions: sway area eyes open was 1200 mm 2 (mean 91 mm 2, range mm 2 in normal subjects); sway area eyes closed was 1556 mm 2 (mean 225 mm 2, range mm 2 in control subjects). No obvious clinical finding could explain this difference. In control subjects there was no statistical difference between head movements measured in HF, HL, and HR conditions. This was true in the eyes open and eyes closed conditions and in the anteroposterior as well as the lateral plane. When comparing mean head sway of the ST group with mean head sway of the control group, significant differences were only observed in the anteroposterior plane. HLD in the ST group was slightly greater (123 mm ± 45 eyes open; 154 mm ± 43 mm eyes closed) than in the control group HL and HR conditions (mean 82 mm ± 16 eyes open; 112 mm ± 21 eyes closed p 0.02). When comparing the ST group with the control group performing the test with head facing forward (HF), the difference was only significant in the eyes open condition (patients 123 mm ± 45; control subjects 88 mm ± 10, p 0.03). Dynamic Balance Task Figure 2A and B shows recordings obtained for lateral sway in a control subject with head facing forward (left panel) and in a left rotation ST patient (right panel). Upper traces show the head sway and lower traces show the pivot sway. Differences in shape between the control subject s and the ST patient s recordings were clearly noticeable. The length of the linear displacement of the pivot (PLD) increased in the patient compared with the control subject. This was true in eyes open and eyes closed conditions but was more pronounced in the eyes FIG. 2. (A and B) Head (upper traces) and pivot (lower traces) lateral sway recorded in one control subject with head facing forward and one patient with a left spasmodic torticollis. The first period of recording with eyes open (EO) is separated by a vertical arrow from the second following period with eyes closed (EC). The length (mm) of PLD and HLD of each recording period is indicated above the corresponding trace. (C and D) Head and pivot anteroposterior sway recorded in one control subject with head facing forward and one patient with a left spasmodic torticollis; same disposition as in A-B.

5 BALANCE IN SPASMODIC TORTICOLLIS 91 closed condition. Similarly, the length of the linear displacement of the head (HLD) increased in the ST patient compared with the control subject and again the differences were more marked in the eyes closed condition. The PLD/HLD ratio was lower in the ST patient than in the control subject for the eyes closed condition (1.16 versus 1.59, respectively) but was similar for the patient and control subject in the eyes open condition (1.46 versus 1.47, respectively). Thus, in the eyes closed condition the control subject attenuated his head movement more efficiently than did the ST patient. Results obtained for anteroposterior dynamic sway from another patient with a left torticollis (Fig. 2D) and a control subject (Fig. 2C) were similar to those obtained for lateral sway, displaying clear differences between the two subjects in both eyes open and eyes closed conditions. Table 2 shows mean values of PLD, HLD, and the PLD/HLD ratio obtained from the control group and the ST group before (ST1) and after (ST2) botulinum toxin treatment in lateral and anteroposterior dynamic sway tests. PLD and HLD tended to be greater in the ST group, before and after botulinum toxin treatment, compared with the control group in eyes open and eyes closed conditions. However, the data only reached significance for lateral sway. The PLD/HLD ratio tended to be lower in the ST group compared with the control group, especially in the eyes open condition, but this only reached significance for lateral sway before botulinum toxin treatment (ST1). Eye closure significantly increased PLD and HLD in both control and ST groups (both before and after botulinum toxin treatment for the latter) and in both planes. An interaction was only observed between subjects and visual conditions for PLD in lateral sway: ST patients were more disturbed by eye closure than were control subjects. The contribution of head position to dynamic balance skill was studied in the control subjects by comparing HF, HL, and HR conditions. Figure 3 shows the mean values of PLD and HLD obtained in the three different conditions with eyes open and eyes closed for lateral and anteroposterior sway. Voluntary rotation of the head to the left or to the right induced a small disturbance in the control subjects only for PLD for lateral sway (p between HF and HR conditions). However, an interaction between the head rotation and vision fac- TABLE 2. Mean values of PLD, HLD, and the PLD/HLD ratio obtained from the control group and the ST group before (ST1) and after (ST2) botulinum toxin treatment in lateral and anteroposterior dynamic sway tests Lateral sway Sagittal sway PLD HLD PLD/HLD PLD HLD PLD/HLD EO 391 ± ± ± 0.4 EO 333 ± ± ± 0.9 Controls Controls EC 700 ± ± ± 0.2 EC 992 ± ± ± 0.6 EO 616 ± ± ± 0.2 EO 426 ± ± ± 0.3 ST1 ST1 EC 1203 ± ± ± 0.3 EC 1203 ± ± ± 0.3 EO 583 ± ± ± 0.3 EO 456 ± ± ± 0.4 ST2 ST2 EC 1125 ± ± ± 0.3 EC 1238 ± ± ± 0.3 Statistical analysis Statistical analysis C/ST1 p p p 0.02 C/ST1 NS NS NS EC/EO p p p 0.02 EC/EO p p NS Interaction p 0.03 NS p 0.01 Interaction NS NS NS C/ST2 p p 0.01 NS C/ST2 NS NS NS EC/EO p p p EC/EO p p NS Interaction p 0.04 NS p 0.04 Interaction NS NS NS ST2/ST1 NS NS NS ST2/ST1 NS NS NS EC/EO p p NS EC/EO p p NS Interaction NS NS NS Interaction NS NS NS Mean values and standard errors of the pivot (PLD), the head (HLD) linear displacements, and the PLD/HLD ratio in control group (n 10) and spasmodic torticollis group (n 10) before botulinum toxin treatment (ST1) and after botulinum toxin treatment (ST2) eyes open (EO) and eyes closed (EC) in lateral and anteroposterior sways. The statistical significance of the differences between the different groups between eyes-open and eyes-closed conditions and the interaction between subjects and visual conditions are indicated in the lower part of the table. NS, not significant.

6 92 M. S. MOREAU ET AL. the eyes closed condition, a comparison was made between PLD and HLD obtained in the left rotation spasmodic torticollis subgroup before botulinum toxin injection and in the control subjects performing the test with their heads voluntarily turned to the left (HL condition). This is illustrated in Figure 4, which shows mean values of PLD and HLD obtained in the two subgroups for lateral sway. Differences between the two groups were obvious and highly significant for both eyes open and eyes closed conditions (PLD: p 0.007, HLD: p 0.002). Despite a statistically significant improvement of head posture in all patients after botulinum toxin treatment (mean score before treatment: 9 ± 3.8, range 5 16; mean score after treatment: 4.6 ± 1.8, range 1 8; p , t 5.04), lateral and anteroposterior PLD and HLD FIG. 3. Mean values and standard errors of head (HLD, A) and pivot (PLD, B), linear displacements (mm) obtained from the control group (n 10) in lateral and anteroposterior sways and in three different conditions: head facing forward (HF clear columns), head turned to the left (HL dark columns), and head turned to the right (HR hatched columns). EO: eyes open; EC: eyes closed. Significant difference between HR and HF or HL and HF conditions are indicated by asterisks (***p <0.001; **p <0.01, *p <0.05). tors was observed: the head rotation effect was only revealed by the closure of the eyes (p between HF and HR conditions, eyes closed; p between HF and HL conditions, eyes closed); it did not reach statistical significance in the eyes open condition. Thus, in the control subjects, the disturbance induced by the voluntary rotation of the head appeared only when the eyes were closed and only for lateral sway. Indeed, head position did not have any influence on anteroposterior balance skill in the control subjects, as illustrated in Figure 3. Because of this minor influence of head rotation on lateral balance skill in the control subjects, particularly in FIG. 4. (A and B) Mean values and standard errors of head (HLD) and pivot (PLD) linear displacements obtained from the left spasmodic torticollis subgroup (n 8, left ST, dark columns) in comparison with the control group turning the head to the left side (n 10 clear columns). Significant difference between the control and patient subgroups are indicated by asterisks (**p <0.01).

7 BALANCE IN SPASMODIC TORTICOLLIS 93 were not significantly different after treatment compared with results obtained before treatment (Table 2). DISCUSSION In this study, we have shown significant differences in dynamic balance parameters between the spasmodic torticollis group and the control group instability is greater in the former than the latter. An increase in dynamic postural body sway in the ST group could have been the result of an increase in head movements, which could have been passively transmitted to the body sway recording device. However, all the patients included in this study had a predominant fixed dystonic posture with a tonic horizontal rotation of the neck to the left or to the right without tremoric, clonic, or other abnormal head movements. Moreover, for lateral sway, head movements measured in static conditions were not statistically different for the ST group compared with the control group. Minor differences were observed for anteroposterior sway. Thus, for lateral sway, involuntary head movements could not have contributed to the greater instability revealed here for ST patients, and for anteroposterior sway they could only be partially responsible for the increased instability. Although voluntary head rotation induced a small disturbance in control subjects (only in the eyes closed condition and only for lateral sway), the alteration of dynamic balance parameters observed in the ST group (in both the eyes open and eyes closed conditions) cannot be entirely explained by the abnormal head rotation alone. Indeed, differences between the ST patients and the control group were observed in both visual conditions and regardless of the head position of the control group (that is, ST group versus HF control group, or left ST subgroup versus HL control group). Moreover, the improvement of the head posture observed in all patients after botulinum toxin treatment was not associated with a significant balance improvement. Balance is a complex biologic function that depends on multiple sensory inputs (from the visual, proprioceptive, and vestibular systems), integrative brain centers, and motor output. 6 The greater instability revealed in ST patients by our sensitive dynamic device could reflect an alteration of input, output, and/or central processing of the balance system. The visual input system remains preserved in cervical dystonia. The proprioceptive system has been recently studied in spasmodic torticollis by means of neck muscles and Achilles tendon vibration. 7 The results suggest that lower limb proprioceptive input remains preserved in spasmodic torticollis, whereas the importance of neck proprioceptive input in whole body postural control seems substantially reduced. There is also increasing evidence that alteration of the central processing of proprioceptive input occurs in dystonia. 8 Thus, it seems likely that impairment of the proprioceptive system contributes to the impairment of dynamic balance skill in ST patients. In addition, it has been suggested that the vestibular system has a role in the pathophysiology of spasmodic torticollis A high incidence of abnormalities in conventional tests of vestibular function has been observed in patients with ST providing evidence of a disturbance of the tonus balance of the vestibulo-ocular system. Whether these abnormalities of vestibular function represent a cause or a consequence of spasmodic torticollis remains unclear. Because, in their study, abnormal vestibulocollic reflexes were not observed in all patients tested and were more commonly observed in patients with a long duration of disease, Colebatch et al. 14 recently suggested that the abnormal responses were an adaptation to the torticollis rather than the cause. Preliminary results, arising from a recent study of ST patients of body sway on a static force platform before and after botulinum toxin injections, show an improvement of some posturographic parameters 6 weeks after botulinum toxin treatment. 15 However, Stell et al. 13 have reported an asymmetric response of the vestibuloocular reflex in a group of ST patients, which persisted despite improvement of head posture, with botulinum toxin injections. This suggests a primary rather than a secondary involvement of the vestibular system in these patients. Further observations arising from a study of cervico-ocular reflexes in ST patients have reinforced the view that vestibulo-ocular asymmetry in ST is unrelated to head posture and is a result of the primary involvement of the vestibular system. 16 Although our method does not provide direct evidence of vestibular dysfunction in ST patients, the absence of changes in dynamic balance parameters after botulinum toxin injection argues in favor of a primary rather than a secondary change in this system. Eye closure altered balance parameters in both groups, but the disturbance was more pronounced in the ST group than in the control group, especially for lateral sway. Suppressing a sensory modality that contributes to balance maintenance allows us to assess its functional importance in the regulation of balance reflexes. Thus, it is probable that vision, in the dynamic balance condition, was predominantly used by ST patients to compensate for their unsteadiness on the platform, especially in the lateral sway direction. Vision is not necessary for balance but it does improve this function. When all sensory channels are available, they usually give congruent and even redundant information, but when one is missing or misfunctioning, the remaining ones become more rel-

8 94 M. S. MOREAU ET AL. evant. That may be the case here with vision for ST patients in the presence of possible vestibular and/or proprioceptive function disturbance. In the control group, HLD length was less than PLD length in both the eyes open and eyes closed conditions. This demonstrates the ability of the body to attenuate body base displacements to attain head stabilization in space. In the ST patients, HLD length was almost equal to PLD length, especially for lateral sway. This could have been the result of an increase in head movements; however, the contribution of this factor has already been discussed and its influence appears limited. Decrease of the PLD/HLD ratio in ST patients more likely reflects an impairment of the head stabilization reflexes, that is, a lack of attenuation of body base displacements at the head level. Differences between the control and ST groups were more obvious in the lateral than in the anteroposterior direction, at least in the dynamic sway tests. This is not surprising, because all the ST patients who took part in this study had clinically predominant abnormal movements of the head in the lateral plane (left or right involuntary rotation). Abnormal movements in the anteroposterior plane (ante- or retroflexion) were absent or mild and infrequent. It is possible that another population of ST patients with predominant involuntary ante- or retroflexion head movements would have had greater unsteadiness in the anteroposterior plane. In static conditions, the body sway of the ST group did not increase significantly in comparison with normal subjects, except in one case. Because our patients did not spontaneously complain of balance disturbances, these results seem to suggest that this conventional posturographic method is not sensitive enough to detect infraclinical balance disturbances in most spasmodic torticollis patients. Incidentally, Wöber et al. 15 using a more sensitive method (firm versus compliant platform) have reported an increase of some body sway parameters in patients with ST compared with control subjects. These differences between static and dynamic posturographic results emphasize the advantage of performing dynamic balance studies to provide a clearer characterization of strategies used, either by individuals or by groups, to actively keep their balance. Acknowledgments: The authors thank Mrs. S. Miailhe for technical assistance and Mrs. C.J.S. Collins for scrutinizing the English. REFERENCES 1. Bessou P, Costes-Salon MC, Dupui PH, Montoya R, Pagès B. Analyse de la fonction d équilibration dynamique chez l homme. Archives Internationale de Physiologie et Biologie 1988;96:3:A Consky E, Basinki A, Belle L, Ranawaya R, Lang AE. The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS): assessment of validity and interrater reliability [Abstract]. Neurology 1990;40(suppl 1): Association Française de Posturologie. Normes 85. AFP Paris, Wright BM. A simple ataxia-meter. Proceedings of the Physiology Society, 1971;218: Freeman MAR, Dean MRE, Hanham IWF. The etiology and prevention of functional instability of the foot. J Bone Joint Surgery [Br] 1965;47: Nashner LM, McCallum G. The organization of human postural movements: a formal basis and experimental synthesis. Behav Brain Sci 1985; Lekhel H, Popov K, Anasastopoulos D, et al. Postural responses to vibration of neck muscles in patients with idiopathic torticollis. Brain 1997;120: Hallett M. Is dystonia a sensory disorder? Ann Neurol 1995;382: Bronstein AM, Rudge P. Vestibular involvement in spasmodic torticollis. J Neurol Neurosurg Psychiatry 1986;49: Bronstein AM, Rudge P. The vestibular system in abnormal head postures and in spasmodic torticollis. In: Fahn S, Marsden CD, Calne DB, eds. Adv Neurol, vol 50. Dystonia 2. New York, NY: Raven Press, 1988: Diamond SG, Markham CH, Baloh RW. Ocular counterolling abnormalities in spasmodic torticollis. Arch Neurol 1988;45: Huygen PLM, Verhagen WIM, Van Hoof JJM, Horstink MWIM. Vestibular hyperreactivity in patients with idiopathic spasmodic torticollis. J Neurol Neurosurg Psychiatry 1989;52: Stell R, Bronstein AM, Marsden CD. Vestibulo-ocular abnormalities in spasmodic torticollis before and after botulinum toxin injections. J Neurol Neurosurg Psychiatry 1989;52: Colebatch JG, DiLazzaro V, Quartarone A, Rothwell JC, Gresty M. Click-evoked vestibulocollic reflexes in torticollis. Mov Disord 1995;10: Wöber CH, Schnider P, Steinhoff N, Zebenholzer K, Auff E. Body sway in patients with spasmodic torticollis before and after botulinum toxin injections. Mov Disord 1996;11(suppl 1):P Stell R, Gresty M, Metcalfe T, Bronstein AM. Cervico-ocular function in patients with spasmodic torticollis. J Neurol Neurosurg Psychiatry 1991;54:39 41.