Effects of galvanic vestibular stimulation on otolithic and semicircular canal eye movements and perceived vertical

Abstract

Objective: The aim of this study was to determine the otolithic and semicircular canal effects of galvanic vestibular stimulation with increasing current strengths on eye movements and the perception of verticality.

Methods: We measured (1) 3-dimensional eye movements, (2) subjective tilt of the peripheral visual field, and (3) subjective tilt of a central vertical line in 12 healthy subjects during galvanic vestibular stimulation. A rectangular, unipolar binaural electric current was applied to each subject's mastoid.

Results: Anodal stimulation of the right mastoid led to an ipsiversive tonic ocular torsion of up to 5.4°, to a contralateral tilt of both the peripheral visual field (1–9°), and a central vertical line (0.5–6.2°) increasing in amplitude with increasing current strengths applied. This reflects otolith stimulation. In most subjects, current strengths of 3 mA or more elicited a slight (horizontal-) torsional nystagmus (amplitude 1–2°) that was superimposed on static torsion. This reflects horizontal and vertical semicircular canal stimulation. A correlation was found in the amount of the 3 measured parameters and the strength of the applied current.

Conclusions: Thus, galvanic vestibular stimulation at low current intensities (1– 3 mA) preferably excites otolith responses, which increase with increasing current intensity. With higher current intensity above 3 mA, additional semicircular canal responses are elicited in the form of horizontal-rotatory nystagmus superimposed on static torsional deviations. The lack of a vertical deviation and nystagmus can be explained by the counterdirected vertical components of the anterior and posterior semicircular canal.

Introduction

Adequate testing of vestibular function depends on active head movements. Head movements, however, always cause a combined stimulation of the vestibular and somatosensory (e.g. cervical receptor) systems (Hood and Kayan, 1985). Therefore, caloric irrigation and galvanic stimulation are often used, since they selectively elicit primarily vestibular stimuli. However, their stimulus cannot be quantified to the same degree as accelerations. Caloric irrigation involves only semicircular canal function (Poilici and Crighel, 1969; Böhmer et al., 1992), while galvanic stimulation most probably involves the entire vestibular endorgan or nerve, i.e. semicircular canal and otolith functions.

In previous human studies it was shown that galvanic stimulation elicits direction-specific body sway (Hlavacka and Njiokiktjien, 1985; Tokita et al., 1989; Inglis et al., 1996), postural electromyographic responses in the arm and leg muscles (Britton et al., 1993), and nystagmic eye movements (Pfaltz, 1967; Brackmann, 1986). The nystagmic eye movements were interpreted to be an effect of the semicircular canal (SCC) function.

Vestibular tone in the roll plane of the vestibulo-ocular reflex is based on the bilateral vestibular input from both the vertical semicircular canals (dynamic effects, nystagmus) (Cohen et al., 1965) and the otoliths (tonic effects, tonic ocular deviation). In the `normal' upright position in the roll plane, the subjective visual vertical is aligned with the gravitational vertical, and the axis of the eyes and the head are horizontal and directed straight ahead. A tonic vestibular tone imbalance results in deviations of eye position and a tilt of the perceived visual scene (Gresty et al., 1992; Dieterich and Brandt, 1993b, Dieterich and Brandt, 1993c; Brandt and Dieterich, 1994), whereas dynamic tone imbalance leads to nystagmus. This tonic tone imbalance in the roll plane can easily be quantified in degrees of ocular torsion and perceived visual tilt (Dieterich and Brandt, 1993a). A pilot study found that galvanic stimulation of the labyrinth with low currents primarily affects tonic otolith function of the vestibulo-ocular reflex in the roll plane (Zink et al., 1997).

The question of whether it is possible to excite otoliths and semicircular canal function separately with the same galvanic stimulation, by simply altering the current strength, is addressed here. We therefore measured tonic otolith effects on eye position (eye deviation, ocular torsion) and perception (tilts of perceived visual vertical), as well as dynamic semicircular canal effects on horizontal, vertical, and torsional eye movements (nystagmus). A clear dissociation of thresholds for tonic and nystagmic eye movements has already been shown for eye movements elicited by head movements and optokinetic stimulation (Greiner et al., 1967).