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Low-Voltage-Activated Potassium Channels Underlie the Regulation of Intrinsic Firing Properties of Rat Vestibular Ganglion Cells

¹Department of Otolaryngology, University of Tokyo School of Medicine, Tokyo; ²Department of Biochemistry and Cellular Biology, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Tokyo; ³Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, Chiba; and ⁴Department of Physiology, Tsurumi University School of Dentistry, Yokohama, Japan

Submitted 10 November 2007; accepted in final form 9 July 2008

Individual primary vestibular afferents exhibit spontaneous activity the regularity of which can vary from regular to irregular. Different aspects of vestibular responsiveness have been associated with this dimension of regularity of resting discharge. Isolated rat vestibular ganglion cells (VGCs) showed heterogeneous intrinsic firing properties during sustained membrane depolarization: some neurons exhibited a strong adaptation generating just a single or a few spikes (phasic type), whereas other neurons showed moderate adaptation or tonic firing (tonic type). Tonic discharging VGCs were rare at postnatal days 5–7 and increased up to 60% of neurons during postnatal 2–3 wk. To explore the major factors responsible for the discharge regularity of primary vestibular afferents, we investigated the contribution of K⁺ channels to the firing properties of isolated rat VGCs. Phasic firing became tonic firing in the presence of 4-aminopyridine or -dendrotoxin, indicating that Kv1 potassium channels control the firing pattern of the phasic VGCs. Tetraethylammonium decreased the number of spikes during step current stimuli in all types. Blockade of Ca²⁺-activated K⁺ channels decreased the number of spikes in tonic VGCs. Our results suggest that Kv1 channels are critical both in determining the pattern of spike discharge in rat vestibular ganglion neurons and in their proportional change during maturation.