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The potassium channel subunit K _V 1.8 ( 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.

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SUBMITTER: Martin HR

PROVIDER: S-EPMC10690164 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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

Martin Hannah R HR Lysakowski Anna A Eatock Ruth Anne RA

bioRxiv : the preprint server for biology 20240818

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, gK,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 KV1 ...[more]

PMID: 38045305

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Project description:Vestibular hair cells (HCs) faithfully and rapidly detect head motions and gravity, driving motor reflexes that stabilize balance and gaze during locomotion. With the transition from water to land, the amniote vestibular inner ear added type I HCs, which differ from amniote type II HCs and anamniote HCs by their large calyx afferent synapse, non-quantal afferent transmission, and a large, low-voltage-activated K+ conductance (gK,L). We recently showed that both gK,L and the major type II K+ conductances (A-type and delayed rectifier) require KV1.8 (Kcna10) subunits. Here we compared KV1.8-null (Kcna10 -/-) and control animals to see how KV1.8 affects function as measured by receptor potentials and nonquantal postsynaptic potentials evoked by direct hair bundle motions, and by vestibulomotor behaviors. Recordings were taken from extrastriolar zones of the utricle. In both HC types, KV1.8 affected receptor potentials by reducing response time and gain, increasing dampening, and expanding the frequency bandwidth toward high frequencies. Effects are most prominent in type I HCs: lowpass corner frequencies of receptor potentials in Kcna10 -/- HCs of both types were ~20 Hz, vs. ~400 Hz in control type I and ~70 Hz in control type II. We recorded nonquantal postsynaptic potentials from extrastriolar calyces, and found that the synaptic transfer function had lower gain and greater phase lag in Kcna10 -/- mice. In behavioral tests, Kcna10 -/- mice had vestibular-ocular reflexes with different response dynamics at low frequencies, impaired performance on a narrow balance beam, abnormal body posture and abnormal head motions in water and on land, and also rarely assumed bipedal stances. These vestibulomotor deficits in Kcna10 -/- mice likely reflect the changes noted in HCs, where KV1.8 expression is concentrated; that is, slower signaling of high-frequency head motions by Kcna10 -/- HCs fails to fully stabilize body and head position during locomotion. Thus, gK,L (KV1.8) contributes to fast signal transmission in the amniote vestibular inner ear and supports improved performance on challenging vestibulomotor tasks.

Dataset Information

The potassium channel subunit K _V 1.8 ( Kcna10 ) is essential for the distinctive outwardly rectifying conductances of type I and II vestibular hair cells.

Graphical abstract

Publications

The potassium channel subunit K<sub>V</sub>1.8 (<i>Kcna10</i>) is essential for the distinctive outwardly rectifying conductances of type I and II vestibular hair cells.

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Dataset Information

The potassium channel subunit K V 1.8 ( Kcna10 ) is essential for the distinctive outwardly rectifying conductances of type I and II vestibular hair cells.

Graphical abstract

Publications

The potassium channel subunit K<sub>V</sub>1.8 (<i>Kcna10</i>) is essential for the distinctive outwardly rectifying conductances of type I and II vestibular hair cells.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets

The potassium channel subunit K _V 1.8 ( Kcna10 ) is essential for the distinctive outwardly rectifying conductances of type I and II vestibular hair cells.