K Channels in Mammalian Vestibular Hair Cells: Facilitating Rapid Signaling of Head Motions

In amniotes, head motions and tilt are detected by two types of vestibular hair cells (HCs) with strikingly different morphology and physiology. Type I HCs appeared in amniotes along with other adaptations to life out of water, likely to support faster vestibular signaling in the air. Mature type I HCs express a large and very unusual potassium conductance, gK,L, which activates negative to resting potential, confers very negative resting potentials and low input resistances, and enhances a unique non-quantal transmission from type I HCs onto their calyceal afferent terminals. The molecular identity of gK,L has been long debated. Following clues pointing to Kv1.8 (KCNA10) in the Shaker K channel family as a candidate gK,L subunit, we compared whole-cell voltage-dependent currents from utricular hair cells of KV1.8-null mice and littermate controls. We found that KV1.8 was necessary not just for gK,L but also for fast-inactivating and delayed rectifier currents in the more ancient type II HCs, which activate positive to resting potential. Kv1.8 accelerated and dampened receptor potentials in both types of hair cells, enhancing their ability to detect rapid head motions. Kv1.8 was essential for extending receptor potential tuning above 20 Hz; information about these higher frequency head motions is critical for maintaining posture, balance, head position, and gaze stability. Kv1.8-null mice had normal motor abilities but struggled on challenging vestibulomotor tasks such as crossing a narrow balance beam and rearing on hindlegs. In the water, where proprioceptive cues are limited, Kv1.8-null mice did not maintain horizontal swim posture or stable head position. These investigations addressed a longstanding mystery about hair cell K channels and their role in type I HC-calyx transmission and vestibular function. Such features that speed up vestibular receptor potentials and non-quantal afferent transmission may have helped stabilize locomotion as tetrapods moved from water to land.