The potassium channel subunit K_V1.8 (Kcna10) is essential for the distinctive outwardly rectifying conductances of type I and II vestibular hair cells

In amniotes, head motions and tilt are detected by two types of vestibular hair cells (HCs) with strikingly different morphology and physiology. Mature type I HCs express an unusual potassium conductance, gK,L, that activates negative to resting potential, conferring very negative resting potentials and low input resistances. These properties distinguish type I HCs from type II HCs in the same vestibular epithelia and from all other HCs. Following unsatisfactory efforts to identify the unusual gK,L channels, clues emerged pointing to KV1.8 (KCNA10) subunits of the Shaker voltage-gated K channel family. With whole-cell recordings from hair cells in utricles of KV1.8-null mice and their wildtype and heterozygote littermates, we show that KV1.8 is necessary for gK,L. Unexpectedly, KV1.8 is also required for the KV conductances of utricular type II HCs: a fast-inactivating A conductance and delayed rectifier that activate positive to resting potential. The distinct properties of the three KV1.8-dependent conductances may reflect different mixing with other KV subunits that are reported to be differentially expressed in type I and II HCs. In HCs of both types, residual outwardly rectifying conductances include KV7 (KCNQ) channels. Current clamp records show that KV1.8-null type II HCs have more electrical resonance and that, in both cell types, KV1.8-dependent conductances speed up and and dampen responses. gK,L's properties may enhance non-quantal transmission onto calyceal afferent terminals, another type I-specific attribute. Such mechanisms to enhance the speed of receptor potentials and afferent transmission may have evolved under pressure from vestibular challenges experienced as vertebrates moved onto land and air.