Elsevier

Brain Research Bulletin

Volume 64, Issue 3, 30 September 2004, Pages 265-271
Brain Research Bulletin

Responses of primary vestibular neurons to galvanic vestibular stimulation (GVS) in the anaesthetised guinea pig

https://doi.org/10.1016/j.brainresbull.2004.07.008Get rights and content

Abstract

Previous studies in humans and animals which have shown that DC galvanic vestibular stimulation (GVS) induces horizontal and torsional eye movements have been interpreted as being due to a preferential activation of primary vestibular afferents innervating the horizontal semicircular canals and otoliths by GVS. The present study sought to determine in guinea pigs whether GVS does indeed selectively activate primary horizontal canal and otolith afferents. Constant-current GVS was passed between electrodes implanted in the tensor-tympani muscle of each middle ear or between electrodes on the skin over the mastoid. During this stimulation, responses from single primary vestibular neurons were recorded extracellularly by glass microelectrodes in Scarpa's ganglion. Afferents from all vestibular sensory regions were activated by both surface and tensor-tympani galvanic stimulation. Tensor tympani GVS was approximately 10 times more effective than surface GVS. At larger current intensities irregularly discharging afferents showed an asymmetrical response: cathodal stimulation resulted in a larger change in firing (increase) than anodal stimulation (decrease), whereas regularly discharging afferents responded symmetrically to the two polarities of GVS. Across all afferents tuned for different types of natural vestibular stimulation, neuronal sensitivity for GVS was found to increase with discharge variability (as indexed by CV*). Anterior canal afferents showed a slightly higher sensitivity than afferents from other vestibular sensory regions. Hence, the present study concluded that GVS activates primary vestibular afferents innervating all sensory regions in a uniform fashion. Therefore, the specific pattern of GVS-induced eye movements reported in previous studies are not due to differential sensitivity between different vestibular sensory regions, but are likely to reflect an involvement of central processing.

Introduction

Constant-current (DC) galvanic vestibular stimulation (GVS) delivered by large surface area electrodes placed over the surface of skin behind the ears is known to induce eye-movement responses in humans (e.g. [12], [18]). Eye movements were observed to consist of tonic and phasic components, and were predominantly torsional and horizontal in direction with smaller vertical deviations. It was presumed that these eye movements were caused by an activation of primary vestibular afferents [8]. Behavioural studies with GVS have been interpreted as showing the pattern of eye movements observed involves combined stimulation of primary vestibular afferents supplying the horizontal semicircular canals (SCC) and otoliths [17]. In order to verify whether this is the case, we have recorded eye movements and responses from single primary vestibular neurons in guinea pigs during GVS.

Galvanic vestibular stimulation conducted in guinea pigs found that 80 μA constant-current GVS delivered through chronically implanted electrodes positioned on the tensor-tympani muscles of the middle ear induced predominantly vertical and horizontal eye movements [11]. This is apparently inconsistent with results from humans and other species, but that inconsistency is resolved because vertical displacement of the eye in lateral-eyed guinea pigs involves activation of similar extra-ocular muscles as torsional displacement of the eye in frontal-eyed humans [16]. Each orthogonal pair of eye muscles was shown to predominantly receive primary vestibular input from vestibular organs having similar geometric orientations [4]. Hence, GVS-induced vertical eye deviation in guinea pigs and GVS-induced torsional eye deviation in humans are likely to reflect similar physiological patterns of primary vestibular afferent activity.

Cathodal galvanic stimulation increases the activity of primary vestibular afferent neurons, whereas anodal galvanic stimulation decreases the activity of these neurons [6]. The normalised sensitivity of these unitary responses (βP*) was shown to depend on discharge regularity [1], [8], [9], where irregularly discharging afferents (CV* > 0.1) were more sensitive to galvanic stimulation than regularly discharging afferents (CV* < 0.1). These previous studies determined the sensitivity of afferents in terms of the change in firing rate (spikes/s) induced by a brief, single constant-current pulse of galvanic stimulation. However, a more reliable measure of galvanic sensitivity was sought in the present study by determining the gain (spikes/s/μA) of primary vestibular afferents over multiple constant-current galvanic pulses of differing amplitudes, and deriving a gain value from the line best fitting all these responses.

Interestingly, in a previous study the firing of more irregularly discharging afferents was silenced during delivery of moderate intensities (up to 100 μA) of anodal galvanic stimulation through perilymphatic electrodes [1], [3], [13]. In one study [1] it was shown that in one irregularly discharging afferent the firing rate increase during cathodal stimulation was greater than the firing rate decrease during the same intensity of anodal stimulation. In comparison, a regularly discharging afferent was shown to respond symmetrically to each polarity of galvanic stimulation. However, no indication of how reliable or widespread this excitatory bias is across neurons and across animals has been provided, and we further sought to obtain such an indication.

Although primary vestibular afferent responses to galvanic stimulation have been examined in some mammals, including squirrel monkeys [8], [9] and chinchillas [1], responses to GVS have not been characterised previously in guinea pigs. The previous studies have provided evidence to suggest that primary vestibular afferents innervating individual vestibular sensory regions respond to galvanic stimulation. However, a direct comparison of the gains of primary vestibular afferents across different vestibular end organs has not been reliably performed.

The present study characterised the sensitivity (or gain) of primary vestibular afferents for constant-current galvanic stimulation applied externally to the inner ear in guinea pigs. External GVS was delivered in the form of surface galvanic stimulation applied over the skin covering the mastoids or through electrodes implanted in the tensor-tympani muscle of the middle ear. The location of the stimulating electrode in the tensor tympani was chosen for three reasons. First, it was a conveniently accessible location that allowed the potentially damaging opening of the labyrinth to be avoided. Second, it was a conductive location very close to the labyrinth, but not in contact with inner-ear perilymph. Third, it allowed electrodes to be implanted permanently to allow galvanic stimulation to be delivered in alert animals in behavioural experiments conducted over a period of up to 2 years.

Section snippets

Subjects

Twenty-two healthy pigmented guinea pigs weighing between 480 and 1200 g were used. The experiments and procedures were followed in accordance with the principles of laboratory animal care (NIH Publication No. 86-23, revised 1985), and were approved by the Animal Ethics Committee (AEC) at the University of Sydney.

Surgical preparation

Animals were anaesthetised using separate intramuscular injections of Nembutal (pentobarbitone sodium 30 mg/kg, Rhone Merieux) and Hypnorm™ (fentanyl citrate 0.22 mg/kg and fluanisone 6.89

Afferent discharge during galvanic stimulation

Time-series plotted in Fig. 1 shows the action potentials discharged by an irregularly firing primary vestibular afferent before, during, and after 5 s pulses of cathodal (−60 μA) and anodal (+60 μA) tensor-tympanic galvanic stimulation. Unilateral anodal stimulation reduced the spike discharge rate of primary vestibular neurons, whereas unilateral cathodal stimulation increased the spike discharge rate. This pattern of activation was observed across all 275 primary vestibular neurons recorded,

Discussion

Constant-current galvanic stimulation delivered through electrodes placed in the tensor tympani muscle of the middle ear or over the surface of skin covering the mastoid was found to induce changes in the activity of primary vestibular neurons at very low intensities. However, surface galvanic stimulation induced roughly the same change in firing rate using approximately 10 times the current intensity of tensor-tympanic GVS. Irregularly firing primary vestibular afferents were consistently

Acknowledgments

We kindly thank Drs. Toshi Murofushi, Darrin Gilchrist, Hamish MacDougall, and Ann Burgess for their helpful involvement and suggestions. This study was funded by the National Health and Medical Research Council (NHMRC) of Australia.

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