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Vestibulopathic gait: you're better off running than walking

Brandt, Thomas

Current Opinion in Neurology: February 2000 - Volume 13 - Issue 1 - p 3-5
Editorial Comment
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Correspondence to Thomas Brandt, Department of Neurology, Ludwig-Maximilians University, Klinikum Grosshadern, Marchioninistrasse 15, 81377 Munich, Germany. Tel: +49 89 70952570; fax: +49 89 70958883; e-mail: tbrandt@brain.nefo.med.uni-muenchen.de

Vestibulopathic gait manifests with disorders of the labyrinth, vestibular nerve, brainstem, archicerebellum, thalamus, or the parieto-temporal cortex. The particular pathological mechanisms that provoke postural and gait instability, even to the point of falls, differ considerably because they may result from changes in otolith or in horizontal or vertical semicircular canal function. Vestibulopathic gait and vestibular falls can be attributed to the particular plane of the affected semicircular canal or a central pathway that mediates the three-dimensional vestibulo-ocular reflex in yaw, pitch, and roll. Ipsiversive falls occur in vestibular neuritis or in Wallenberg's syndrome, in which they are known as lateropulsion. Contraversive falls are typical of the otolith Tullio phenomenon, vestibular epilepsy and thalamic astasia. A predominant fore-aft instability is observed in bilateral vestibulopathy, benign paroxysmal positioning vertigo, as well as in downbeat or upbeat nystagmus syndrome. Falls can be diagonally forwards (or backwards) and towards or away from the side of the lesion, depending on the site of the lesion (the ocular tilt reaction is ipsiversive in peripheral vestibular and medullary lesions, but contraversive in mesencephalic lesions), and on whether vestibular structures are excited or inhibited.

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Is slow motion safer than fast motion in acute vestibulopathy?

If an acute unilateral peripheral vestibular failure causes a distressing vestibular tone imbalance, the afflicted individuals move slowly, grasp searchingly for support, or must be guided in order to correct for their deviating gait and lateral falls. Slow motion is commonly believed to be much safer for these patients than fast motion. When walking slowly, the area of foot support is larger (both feet on the ground) than when running (one foot on the ground at a time). One would thus expect balance control to rely more on the actual vestibular input during running.

A chance observation of a dog with acute left unilateral vestibular failure, however, showed us that running is safer [1]. After awakening one day, the dog suddenly showed a severe postural imbalance and repeatedly fell to the left. When she stood still, head movements caused the falls. When walking slowly, she veered to the left, staggered about in counterclockwise circles and repeatedly fell. Surprisingly, once the dog was outside and began to trot, she was suddenly able to move without deviating from her course, and obviously felt better and more confident as her raised, wagging tail indicated. However, as soon as she stopped trotting and began to walk slowly she again showed the severe tendency to deviate from her intended path and fell to the left.

If patients with acute vestibular neuritis are requested to close their eyes and slowly walk or run straight ahead, they show a direction-specific deviation of gait towards the affected ear. However, they maintain their direction much better when running [1]. Increased walking speed also has a clearly stabilizing influence on their balance and maintenance of the intended path. Furthermore, if healthy volunteers with a post-rotatory transient vestibular tone imbalance are asked either to walk slowly or run straight ahead while blindfolded, mean deviation is significantly smaller when running (Fig. 1) [1].

Figure 1

Figure 1

It is also possible to induce a transient vestibular tone imbalance by using binaural galvanic vestibular stimulation, which causes an apparent tilt sensation to the cathodal side and a deviation of gait towards the anodal side [2]. Again, the angle of deviation is significantly smaller when running, but there is no difference in mean deviation for walking or running when patients or volunteers walk or run in place without locomotion (K. Jahn, et al., in preparation).

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Automatic spinal locomotor pattern is largely independent of actual vestibular input

Earlier reports in the literature demonstrate that the actual control of the vestibular system can be bypassed. For example, blindfolded patients with bilateral vestibular failure are able to perform linear goal-directed locomotion towards memorized targets [3]. Automatic locomotor patterns have been found in the chronic spinal cat (for review see [4]) and in paraplegic patients whose body weight was partly unloaded during suspension from a parachute harness connected to an overhead crane while walking on a moving treadmill [5]. This locomotor pattern is distinct from spinal stretch reflex activity and can be improved by training [6]. Therefore, although spinal pattern generators can initiate locomotion, spinal locomotion is far from perfect and lateral stability is poor. For optimized locomotion, supraspinal motor control and the integration of afferent and re-afferent sensory input are necessary. Different regions in the vertebrate brainstem and cerebellum (e.g. the mesencephalic, subthalamic, pontine, and cerebellar locomotor areas) have been shown to be capable of supraspinal initiation and modulation of locomotion [7]. Vestibular input is not necessary to initiate and maintain the locomotor pattern, but rather to stabilize balance and to continue in the intended direction by virtue of descending vestibulospinal, rubrospinal, and reticulospinal signals. This becomes particularly important during body perturbations and under conditions of a vestibular tone imbalance.

A functional interpretation of the observation that you're better off running than walking with acute vestibulopathy would argue that an automatic spinal programme of locomotion triggers the inhibition of descending vestibular sensory inflow. This explanation would agree with the recently proposed concept of sensory down- and up-channelling for multisensory postural control. According to this theory, the vestibular organ is the body's sensor of position, i.e. it receives the ‘body-in-space’ signals (down-channelling), and the somatosensory system measures the joint angles, i.e. it receives the ‘support-in-space-tilt’ signals (up-channelling) [8]. In our examples, the ascending rather than the descending signals would define the desired value for the joints to control posture. A misleading vestibular signal could thus be suppressed via down- and up-channelling.

Further evidence in the literature supports this functional interpretation. Like the vestibular system, the somatosensory system can also be inhibited. Monosynaptic stretch reflex responses in the human leg, for example, are suppressed and ascending spinal group I afferents are inhibited during passive and active movement [9]. Moreover, the ability to detect a muscle twitch was reported to be attenuated when humans move [10]. These findings are consistent with a general attenuation of sensory feedback during movement and locomotion.

The multisensory-sensorimotor interaction necessary for postural control is, thus, not a simple fusion, but rather a complex of different processes that are fine-tuned by repetition and learning. How they interact is influenced not only by the pattern of actual motion stimulation, but also by the particular postural and locomotor tasks. This is reflected by the differential effects that an actual vestibular tone imbalance has on slow walking and running as well as on walking and running in place without locomotion. Control of slow walking obviously depends on afferent and re-afferent sensory input to a larger extent than does fast walking or running. It makes sense to suppress the vestibular (or somatosensory) input once a highly automatic motor pattern of fast walking or running has been initiated. Otherwise, the (re-afferent) sensory stimulations caused by head and joint motion during locomotion would interfere, acting like adverse feedback, and modify an already optimized automatic programme. However, there are also conditions in which the suppression of vestibular input is not desirable, for example, in the case of unexpected perturbations that bear the risk of sudden falls. It has recently been shown that when the environmental context changes, the natural perturbations received by the ankles during walking, the Ia afferents, momentarily increase their firing rate to a level that cannot be suppressed by presynaptic inhibition [11,12].

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Conclusion

It seems most likely that vestibular control of balance and locomotion can be modulated in two ways: it is inhibited during automatic fast walking or running but disinhibited in the case of unexpected perturbations. These findings on the differential effects of an acute vestibulopathy on walking or running may have important consequences for the physical therapy and rehabilitation of patients with vestibulopathic gait.

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References

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© 2000 Lippincott Williams & Wilkins, Inc.