Perceptual and oculomotor effects of neck muscle vibration in vestibular neuritis. Ipsilateral somatosensory substitution of vestibular function.

Brain (1998), 121, 677–685 Perceptual and oculomotor effects of neck muscle vibration in vestibular neuritis Ipsilateral somatosensory substitution of vestibular function Michael Strupp,1 Victor Arbusow,1 Marianne Dieterich,1 Wolfram Sautier2 and Thomas Brandt1 Departments of 1Neurology and 2Oto-Rhino-Laryngology, University of Munich, Klinikum Grosshadern, Munich, Germany Correspondence to: Dr Michael Strupp, Department of Neurology, University of Munich, Klinikum Grosshadern, Marchioninistrasse 15, 81366 Munich, Germany Summary Afferent cervical somatosensory input may substitute for absent vestibular information as part of central vestibular compensation after unilateral peripheral vestibular deficit. In order to determine the particular contribution of neck muscle spindles to the perception of body orientation and to the oculomotor system, we measured (i) the subjective visual straight ahead (SVA) by psychophysical tests and (ii) the changes in eye position by video-nystagmography during unilateral stimulation of the posterior neck muscles by vibration (100 Hz). Twenty-five patients with subacute unilateral vestibular lesion (vestibular neuritis) and 25 controls participated in the study. Vibration elicited a horizontal displacement of SVA towards the side of stimulation in all subjects. Mean displacement (6 SD) was 3.28 6 2.96° for right-side and 3.45 6 2.93° for left-side stimulation in controls. Muscle stimulation on the patients’ lesion side induced a significantly higher displacement (11.51 6 6.63°) than contralateral stimulation (3.04 6 2.95°, P , 0.01, paired Student’s t test). The mean difference during stimulation between the two sides in the patients was 8.02 6 5.52°; in the controls, however, it was only 0.74 6 0.47° (P , 0.001, Student’s t test). This asymmetry increased gradually in patients over a period of weeks, reaching a maximum at days 60–80 and declining thereafter. Video- nystagmography revealed that ipsilateral stimulation in patients induced large horizontal eye deviations of up to 25° towards the side of the lesion (9.1 6 7.6°, n 5 18). Contralateral stimulation induced only small shifts, which were within the range of controls. The correlation coefficient between displacement of the SVA and change in eye position was high (r 5 0.94, P , 0.0001), indicating that the shift of SVA is the perceptual correlate of the directional change of gaze in space. This interpretation was supported by two control experiments in which the subject was required to (i) indicate the subjective straight ahead by finger-pointing with the eyes closed and (ii) adjust SVA when looking through horizontally reversing prisms. Vibration of neck muscles caused almost no displacement of the SVA when it was indicated by pointing with the eyes closed, but reversed the direction of the displacement if the subject wore reversing prisms. In summary, our data showed: (i) an increase in muscle spindle input following unilateral vestibular lesion; (ii) this increase is asymmetrical, restricted to the affected side, and gradually builds up over weeks; and (iii) the perceived effects during vibration are secondary to changes in eye position rather than changes in cortical representation of body orientation. This is the first study to demonstrate a unilateral increase in somatosensory weight, which substitutes for missing vestibular input. Keywords: vestibular neuritis; central compensation; cervico-ocular reflex; subjective straight ahead; neck muscle vibration Abbreviations: PIVC 5 parieto-insular vestibular cortex; SVA 5 subjective visual straight ahead Introduction Unilateral peripheral vestibular failure causes a distressing vestibular tone imbalance with rotational vertigo, spontaneous horizontal rotatory nystagmus away from the affected side, and postural imbalance with falls towards the affected side. This tone imbalance is readjusted by central compensation, © Oxford University Press 1998 which involves multiple processes in distributed neuronal networks at different locations with different time courses (Fetter and Zee, 1988; Curthoys and Halmagyi, 1995; Dieringer, 1995; Brandt et al., 1997). Since central compensation of peripheral vestibular lesions is less perfect 678 M. Strupp et al. than generally believed, other additional mechanisms must subserve the functionally insufficient compensation. One such mechanism is sensory substitution (Curthoys and Halmagyi, 1995). Proprioception and vision may substitute for parts of the missing vestibular input to allow better gaze stabilization during head movements (Dichgans et al., 1973; Gresty et al., 1977). For example, neck afferents provide information about head position, and the cervical proprioceptive system is especially important for body orientation (Magnus, 1924; Mergner et al., 1991, 1992; Hlavacka et al., 1996). The cervical proprioceptive system can be stimulated by neck muscle vibration (Biguer et al., 1988; Taylor and McCloskey, 1991; Karnath, 1994; Karnath et al., 1996; Popov et al., 1996; Lekhel et al., 1997), which elicits, for example, displacements of the subjective straight ahead. It is difficult to separate the amount of somatosensory and visual substitution along the time course of central vestibular compensation in a patient with unilateral vestibular deficit. Vibration of unilateral neck muscle has different effects on spatial orientation and eye position, which may, however, indicate changes in the cervical proprioceptive input. In this study the following questions were addressed: (i) is there a (possibly side-specific) increase in the cervical proprioceptive influence on perception – measured by the subjective visual straight ahead (SVA) – and on the horizontal eye position in patients with unilateral vestibular deficit? (ii) if there is an increased influence on perception, what is the underlying mechanism? (iii) what is the time course of these changes? Method Patients and controls We examined 25 patients with subacute vestibular neuritis and persisting vestibular deficit (13 males and 12 females aged 17–81 years, mean 6 SD 5 50.2 6 12.3 years) and 25 age-matched, healthy control subjects (14 males and 11 females aged 49.1 6 14.2 years). Thirty-five of the initial 60 patients with vestibular neuritis recovered within the first 3 weeks and were therefore excluded. All subjects gave their informed written consent to participate in the study according to the guidelines of the Ethics Committee of the Medical Faculty of the University of Munich. The experiments were done in accordance with the Helsinki II Declaration. The diagnosis of vestibular neuritis was based on (i) the patient’s history (acute/subacute onset of severe prolonged rotational vertigo and nausea), (ii) clinical and neuro-ophthalmological examinations (horizontal–rotatory spontaneous nystagmus towards the unaffected ear without evidence of a central vestibular lesion, pathological bedside testing of high-frequency vestibulo-oc (...truncated)