Elsevier

Experimental Neurology

Volume 202, Issue 1, November 2006, Pages 21-35
Experimental Neurology

Postural responses to multidirectional stance perturbations in cerebellar ataxia

https://doi.org/10.1016/j.expneurol.2006.05.008Get rights and content

Abstract

Previous studies of patients with focal cerebellar damage underscored the importance of the cerebellum for balance control. These studies were restricted to postural control in the pitch plane, and focused mainly on leg muscle responses. Here, we examined the effect of degenerative cerebellar lesions on postural control in multiple directions, and studied how such lesions affect intersegmental coordination of the legs, trunk and arms. We formulated two main questions. (a) Do patients with cerebellar ataxia predominantly have balance problems in the sagittal or frontal planes? (b) Is instability in cerebellar ataxia associated with increased joint motion or with reduced joint motion? We selected nine patients with autosomal dominant spinocerebellar ataxia (SCA) – three with pure ataxia and six with mild extra-cerebellar features – and 12 matched controls. Upright standing subjects received support surface rotations (7.5° at 60°/s) that were randomly delivered in eight different directions of pitch or roll. We used full body kinematics to determine displacements of the center of mass (COM) and of individual body segments. We also collected surface EMG from 10 leg, trunk and arm muscles. Primary variables of interest were COM displacement and trunk control (angles and muscle responses). Secondary analyses focused on angles and muscle responses of the legs and arms. COM analysis demonstrated that SCA patients had greatest instability following backward and laterally directed perturbations. Major factors in causing this instability were, first, a marked reduction of stimulus-induced knee flexion and, second, excessive “hypermetric” motion of the pelvis (in roll) and trunk (in pitch). Muscle responses of SCA patients were characterized by increased late balance correcting activity. Responses of patients with pure ataxia were comparable to those of patients with mild extra-cerebellar features. A main underlying cause of postural instability in SCA patients appears to be “locking” of the knees, which may reflect compensation (by reducing interaction between body links) or reduced vestibulocerebellar control over leg muscles. The observed pathophysiology is very different from that seen in other patient populations.

Introduction

Re-establishing upright posture when balance is perturbed is a complex process. One approach to gain more insight into the underlying physiology of normal balance control is to examine mechanisms of instability in patients with selective lesions. This approach assumes that by examining the clinical effects of a focal lesion, one can estimate the normal function of the lesioned brain area, provided there is no compensation through other central nervous system regions. Following this approach, several studies have examined patients with ataxia caused by lesions in the cerebellum. One conclusion reached was that cerebellar damage causes increased postural sway during stance (Mauritz et al., 1979, Diener and Dichgans, 1992). A second conclusion was that cerebellar ataxia patients cannot scale the size of their postural responses to perturbations of stance, as they tend to over-respond (Diener et al., 1984, Horak and Diener, 1994, Timmann and Horak, 1997). Cerebellar ataxia patients had no problems with timing of their postural responses (Horak and Diener, 1994), although clinical impressions suggest that timing problems may contribute to movement abnormalities in cerebellar disease.

Additional insights in balance control of cerebellar ataxia patients might be gained using new dynamic posturography techniques. Previous studies used dynamic posturography delivering postural perturbations to stance along the pitch plane. Until now, no study has examined balance control of cerebellar ataxia patients to perturbations in the roll plane, or to multidirectional perturbations with combined roll and pitch stimuli, though the wide-based gait of cerebellar ataxia patients and their problems with tandem gait suggest that patients mainly have problems with balance control in the roll plane. A recent quantitative study of trunk movements during everyday walking and stance tasks revealed that cerebellar ataxia patients have predominant instability in the anterior–posterior plane (van de Warrenburg et al., 2005a), but in daily life, cerebellar ataxia patients fall in all directions (van de Warrenburg et al., 2005b).

Additional new insights into spinocerebellar ataxia (SCA) might be gained by studying a more comprehensive set of balance measures compared to previous work, which was mainly focused on lower leg muscles acting on the ankle joint. Several studies underscored the additional importance of knee, trunk and arm responses for balance control (Cresswell et al., 1994, Aruin et al., 2001, Carpenter et al., 2004a). For example, the significance of trunk responses was demonstrated in a comparative study of young and elderly subjects who were exposed to multidirectional balance perturbations (Allum et al., 2002). When a support surface suddenly tilted sideways, young healthy persons initially had a lateral flexion response over the first 150 ms, so the upper trunk rolled in the opposite direction to platform roll. In contrast, for elderly subjects, this initial trunk roll was negligible. If the characteristic hypermetria of cerebellar ataxia is also present in the trunk, we would expect to find exaggerated trunk movements during balance corrections. On the other hand, it is also possible that cerebellar ataxia patients co-activate their trunk muscles in order to stiffen their trunk and thereby reduce trunk motion. A fear of falling – which is common in cerebellar ataxia patients (van de Warrenburg et al., 2005b) – is associated with such reactions in anticipation of postural perturbations (Carpenter et al., 2001b). Another reason to reduce movements of the trunk would be to facilitate motor control by reducing the number of interactions between body links. Cerebellar ataxia patients typically resort to this strategy in an attempt to reduce hypermetria (Thach et al., 1992, Bastian et al., 2000).

To address these issues, we performed a detailed posturography study in cerebellar ataxia patients. We formulated three specific questions. First, in which directions are patients mostly unstable? To answer this question, we examined displacements of COM and body segments in response to postural perturbations in multiple directions (pitch, roll, or both). Second, we were interested to see if postural instability in cerebellar ataxia would be related to increased or reduced intersegmental movements. For this purpose, we examined the kinematic profiles of individual body segments. Third, to better understand the observed changes in kinematic profiles, we examined surface EMG responses of leg, trunk and arm muscles.

Section snippets

Subjects

We selected nine patients with genetically proven autosomal dominant spinocerebellar ataxia (SCA) whose clinical presentation was dominated by cerebellar ataxia, and without prominent extracerebellar signs (such as spasticity or extrapyramidal features) that would affect balance (Table 1). All patients were personally examined by a neurologist specialized in cerebellar ataxia (H.P.H.K. or B.W.W.), followed by a second careful examination by a movement disorders specialist (B.R.B.). We screened

COM displacements

All subjects had COM displacements in the same direction as the platform perturbation. In the A–P plane, pure backward perturbations caused larger backward COM displacement in patients than controls (Fig. 1A). Around 600 ms, A–P COM movement of controls had reached a plateau whereas COM of patients continued to move backwards. The average A–P COM displacement at 800 ms for all perturbation directions is shown in Fig. 1B. Statistical analysis indicated that COM displacement was differently

Discussion

These results provide new insights into the nature of balance impairment in ataxia patients, and point to a specific underlying pathophysiological mechanism that is different from that seen in other patient populations (Carpenter et al., 2001a, Carpenter et al., 2004a, Bloem et al., 2002, Allum et al., 2002). Our main findings were as follows. SCA patients had greatest instability following both laterally and backward directed perturbations. The major factors in causing this instability seemed

Acknowledgments

This research was supported by the Internationaal Parkinson Fonds (to M. Bakker), by Swiss National Research Foundation grant 31.59319 and 31.104212/1 (to J.H.J. Allum), by the Prinses Beatrix Fonds (to J.E. Visser) and by a research grant from the Radboud University Nijmegen Medical Centre, The Netherlands (to B.P. van de Warrenburg).

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