Galvanic vestibular stimulation in humans: effects on otolith function in roll

Galvanic vestibular stimulation in humans: effects on otolith function in roll

Neuroscience Letters 232 (1997) 171–174 Galvanic vestibular stimulation in humans: effects on otolith function in roll Reto Zink*, Sven Steddin, Alex...

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Neuroscience Letters 232 (1997) 171–174

Galvanic vestibular stimulation in humans: effects on otolith function in roll Reto Zink*, Sven Steddin, Alexander Weiss, Thomas Brandt, Marianne Dieterich Department of Neurology, Klinikum Grosshadern, Marchioninistrasse 15, 81377 Munich, Germany Received 8 July 1997; received in revised form 7 August 1997; accepted 8 August 1997

Abstract The effects of unilateral galvanic vestibular stimulation on (1) ocular torsion, (2) subjective tilt of the peripheral visual field, and (3) subjective tilt of a foveal vertical line were measured in 12 healthy subjects. A rectangular, unipolar binaural electric current was applied to the subject’s mastoid. Anodal stimulation of the right mastoid led to an ipsiversive tonic ocular torsion (0.5–3.7°) and to a contralateral tilt of both the peripheral visual field (1–9°), and a foveal vertical line (0.5–6.2°). There was a correlation between the amount of the three measured parameters and the strength of the applied current. Static ocular torsion, central and peripheral visual tilts represent stimulusinduced tonic otolith imbalance between the two labyrinths. Thus, galvanic vestibular stimulation not only affects dynamic semicircular canal input but also static otolith input in the roll plane.  1997 Elsevier Science Ireland Ltd. Keywords: Galvanic stimulation; Subjective tilt of the visual field; Otoliths; Ocular torsion; Graviceptive pathways; Human

In previous human studies it was shown that galvanic stimulation elicits direction-specific body sway [11,12,19], postural electromyographic responses in the arm and leg muscles [3], and nystagmic eye movements [1]. The aim of this study was to determine the differential effects of galvanic stimulation on tonic otolith function of the vestibulo-ocular reflex in the roll plane. A tone imbalance in the roll plane can easily be quantified in degrees of ocular torsion and perceived visual tilt [9]. Vestibular tone in roll plane is based on the bilateral input from both the semicircular canals (dynamic effects, nystagmus) and the otoliths (tonic effects, tonic ocular deviation). In the ‘normal’ upright position, the subjective visual vertical is aligned with gravitational vertical, and the axes of the eyes and the head are horizontal. This study was comprised of 12 subjects (8 males, 4 females, mean age 30.8 years, range 25–46 years) without any history of cochlear, vestibular or central nervous system disorders. Grass gold electrodes (5 mm in diameter) taped to both mastoid processes were used to apply a rectangular, unipolar binaural electric current (1.5–3.0 mA; direct cur* Corresponding author. Tel.: +49 89 70906119; fax: +49 89 70906101; e-mail: [email protected]

rent (DC)) between both mastoids seven times at 10 s intervals. At least two different current intensities were used, chosen individually so as not to cause any discomfort. Polarity was changed between the different test trials. Ocular torsion of both eyes was measured separately by (1) video recordings of the fundus with the laser scanning ophthalmoscope (Rodenstock, Germany) and by (2) videooculography technique. Ocular torsion (in degrees) was calculated from 4–6 fundus photographs taken from the online video recording as the mean angle between a straight line through the papilla and fovea (papilla-fovea meridian) and the horizontal line (for details, see Dieterich and Brandt [4]). In addition, in three subjects three-dimensional video recordings [16] of each eye were made during stimulation periods (Fig. 1). For psychophysical measures of perceived tilts, the subject sat with his/her head in an upright position in front of a half-spherical dome 60 cm in diameter. The surface of the dome extended to the limits of the observer’s visual field, and did not contain any gravitational cues. A central black target with a white line subtended 14° of visual angle at a distance of 30 cm to the eyes. This central test edge had to be adjusted after stimulation according to the perceived tilt during stimulation (central foveal tilt).

0304-3940/97/$17.00  1997 Elsevier Science Ireland Ltd. All rights reserved PII S0304- 3940 (97 )0 0610- 1

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Fig. 1. Original video-oculographic recordings of torsional, vertical, and horizontal movements of the left eye during galvanic vestibular stimulation; black bars indicate stimulation periods with 3.5 mA DC current. Yaxis, torsional, vertical and horizontal components of eye position in degrees. The anode was placed on the left mastoid. Direction of eye movements is shown from the subject’s point of view.

To measure subjective tilts of the peripheral visual field, in a second session, apparent tilt of the half-spherical dome was indicated by the subject rotating the dome after the stimulation according to the perceived tilt during stimulation. The combination of both measures, the central ‘foveal’ tilt and the peripheral dome tilt, allowed determination of the stimulus-induced visual tilt for the central and peripheral retina. To measure eye movements, video monitoring of the fundus during galvanic stimulation (1.5–3.0 mA) showed single nystagmus beats in 5 of 12 subjects (1–3 oscillations at a small amplitude of about 2°). Direction was always horizontal, with the quick phase toward the cathode. In all subjects anodal stimulation on the right induced a static intorsion of the left eye 1.68 ± 0.80° (range 0.5–3.1°); anodal stimulation of the left ear induced an extorsion of the left eye of 1.40 ± 0.54° (range 0.5–2.2°) (Table 1). In four subjects static ocular torsion was recorded in both eyes successively during galvanic vestibular stimulation. The ipsiversive direction and the amplitude of the induced static ocular torsion was the same for both eyes in all subjects

(paired t-test) with interindividual differences in the amplitudes. To measure subjective visual dome tilts, in all subjects anodal stimulation on the right led to a visual field tilt to the contralateral left (counterclockwise from the subject’s point of view); anodal stimulation on the left led to a visual field tilt to the right (clockwise). Tilt amplitudes varied interindividually, e.g. perceived tilt during stimulation with 2 mA ranged from 1.3–6.3° (Table 2). This variability was largest for stimulation at 2.5 mA and decreased with higher current strength. Data were symmetric for anodal stimulation of the right and the left mastoid at all current strengths (paired ttest). The strength of the applied current was correlated with the tilt amplitude (r = 0.59). T-test revealed significant differences (P , 0.05) for tilts with stimulation of 2 and 3 mA for both sides. To measure central ‘foveal’ tilts, during anodal stimulation of the right ear, tilts of the central test edge to the left were induced by 1.3° (range 1.0–6.2°). For anodal stimulation of the left ear tilts were 0.7° (range 0.5–2.0°) to the right. A paired t-test revealed significant differences between the adjustment with the anode on the right and the anodal stimulation on the left side as well as between the reference measurement and the adjustment during galvanic stimulation with the anode on the right side (P , 0.05). Which vestibular structures are stimulated? In 1820 Purkinje [14] was the first to describe the effects of galvanic stimulation on eye movements and posture. He reported on regularly induced horizontal-rotatory nystagmus and concluded that galvanic stimulation mainly affects the semicircular canal (SCC) function. However, it is still not clear which portions of the labyrinth and/or the vestibular nerve are activated by galvanic stimulation. Studies in the squirrel monkey have shown that externally applied galvanic currents modulate the tonic firing rate of vestibular afferents by acting directly on the vestibular afferents close to their postsynaptic trigger site [8]. Thus, this broad-based stimulation is believed to act primarily on the fibres of the vestibular nerve. Cathodal currents increase and anodal currents suppress vestibular afferent spike activity [13]. Consequently galvanic stimulation is analogous to caloric irrigation or rotational stimulation, since cathodal current, warm water irrigation, and ipsiversive acceleration all induce increases in vestibular afferent activity. Most of the present studies on galvanic stimulation have

Table 1 Static ocular torsion [°] with galvanic stimulation of the right and left mastoid Left eye (n = 12)

Side of stimulation

Right Left

Right eye (n = 4)

Mean ± SD

Minimum

Maximum

Mean ± SD

Minimum

Maximum

1.68 ± 0.80 1.40 ± 0.54

0.50 0.50

3.10 2.20

1.56 ± 0.90 1.62 ± 0.55

0.48 0.60

2.65 1.90

SD, standard deviation.

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R. Zink et al. / Neuroscience Letters 232 (1997) 171–174 Table 2 Influence of the strength of the applied current on the amount of the subjective visual tilt [°] Current strength (mA)

na

Stimulation right Mean ± SD

1.5 2.0 2.5 3.0 a

4 12 12 4

2.02 2.67 3.18 4.92

± ± ± ±

0.87 1.44 2.28 1.51

Stimulation left Minimum

Maximum

Mean ± SD

1.31 1.29 1.16 2.97

3.26 6.34 9.41 6.50

1.68 2.63 3.13 4.84

± ± ± ±

0.46 1.21 2.00 1.74

Minimum

Maximum

1.34 1.01 1.01 2.59

2.33 5.78 8.47 6.37

Number of subjects examined; SD, standard deviation.

concentrated on its effects on posture [12] and nystagmus [1]. Low currents seem to induce postural effects, higher currents effect eye movements [18]. Nystagmus was characterized as horizontal-rotatory with the slow phase towards the anode and elicited regularly with currents of about 7 mA [1]. Posturography revealed a direction-specific lateral body sway toward the anode, parallel to a line between both labyrinths, which persisted according to this line when the subject turned his head or his trunk and head [19]. All these effects could not be attributed to specific vestibular afferents, SCCs or otoliths. Due to the methodological limitations of techniques for recording torsional eye movements, previous studies concentrated on horizontal and vertical nystagmic eye movements. The measurement of static ocular torsion by means of fundus photographs and video-oculography and the determination of perceived visual tilt permit quantification of tonic vestibular imbalance in the roll plane, which is commonly considered as an otolith function. Two new findings from our study on galvanic vestibular stimulation are relevant for the functional differentiation of the peripheral vestibular afferents: (1) the tonic binocular torsion of about 0.5–3.7° toward the anode and (2) the perceived stimulusinduced tilt of a vertical line or the perceived room tilt of about 1.0–9.4° in the opposite direction. Both indicate a stimulus-induced tonic otolith tone imbalance. Contrary to earlier studies, which induced nystagmus with higher currents, we only observed single nystagmus beats during or at the end of the tonic eye deviation. Lower currents (1.5–3.0 mA) seem to elicit predominantly tonic otolith effects. This raises the question, if it is possible to stimulate otolith or semicircular canal function selectively by using either low or high currents. The evidence for otolith involvement in the roll plane is based on earlier studies in patients who presented with tonic ocular torsion and significant deviations of the perceived visual vertical [9]. These patients suffered from a peripheral vestibular disorder (vestibular neuritis [15]; stapedectomy [10]) or a unilateral central vestibular lesion of the otolith pathways within the brainstem [2,5,6]. The rare case of a patient with an otolithic Tullio phenomenon, a pathological, direct mechanical stimulation of the utricle, gave comparable ocular motor and perceptual results [7]. This patient showed tonic torsional eye deviations and perceptual tilts of

a vertical line during repetitive acoustic stimulation, which were similar to animal responses during repetitive galvanic stimulation or electrical stimulation of the utricular nerve [17]. Thus, galvanic vestibular stimulation not only affects dynamic SCC input but also static otolith input in roll. The direction of ocular motor and perceptual tilts is ipsiversive to anodal and contraversive to cathodal stimulation. We wish to thank Mrs. C. Frenzel for orthoptic assistance and Mrs. J. Benson for copy editing. This work was supported by the Deutsche Forschungsgemeinschaft, Klinische Forschergruppe, Nr 639/5-1, and the WilhelmSander-Stiftung.

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