The potassium channel subunit KV1.8 (Kcna10) is essential for the distinctive outwardly rectifying conductances of type I and II vestibular hair cells

Abstract

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 a large and very unusual potassium conductance, g K,L , which activates negative to resting potential, confers very negative resting potentials and low input resistances, and enhances an unusual non-quantal transmission from type I cells onto their calyceal afferent terminals. Following clues pointing to K V 1.8 (KCNA10) in the Shaker K channel family as a candidate g K,L subunit, we compared whole-cell voltage-dependent currents from utricular hair cells of K V 1.8-null mice and littermate controls. We found that K V 1.8 is necessary not just for g K,L but also for fastinactivating and delayed rectifier currents in type II HCs, which activate positive to resting potential. The distinct properties of the three K V 1.8-dependent conductances may reflect different mixing with other K V 1 subunits, such as K V 1.4 (KCNA4). In K V 1.8-null HCs of both types, residual outwardly rectifying conductances include K V 7 (KCNQ) channels.Current clamp records show that in both HC types, K V 1.8-dependent conductances increase the speed and damping of voltage responses. Features that speed up vestibular receptor potentials and non-quantal afferent transmission may have helped stabilize locomotion as tetrapods moved from water to land.