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

Abstract

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 (+/- SD) was 3.28 +/- 2.96 degrees for right-side and 3.45 +/- 2.93 degrees for left-side stimulation in controls. Muscle stimulation on the patients' lesion side induced a significantly higher displacement (11.51 +/- 6.63 degrees) than contralateral stimulation (3.04 +/- 2.95 degrees, P < 0.01, paired Student's t test). The mean difference during stimulation between the two sides in the patients was 8.02 +/- 5.52 degrees; in the controls, however, it was only 0.74 +/- 0.47 degree (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. Videonystagmography revealed that ipsilateral stimulation in patients induced large horizontal eye deviations of up to 25 degrees towards the side of the lesion (9.1 +/- 7.6 degrees, n = 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 = 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.