IK,L properties of vestibular Type I hair cells are affected by the nerve calyx ending

Mammalian vestibular epithelia have a distinctive sensory cell , called Type I hair cell, that is contacted by an afferent calyx enveloping the entire cell basolateral membrane. Type I cells express a signature low-voltage-activated outward rectifying K+ current, IK,L, which is responsible for their low input resistance at rest . Despite its functional importance, however, IK,L biophysical properties and molecular profile have not yet been defined. Its voltage- and time-dependent properties have been reported to vary at different developmental stages, among cells at a same age, and also over time in the same cell. By using patch-clamp recording from in situ and dissociated mouse crista Type I cells, we found that the observed variability in IK,L properties may be accounted for by different degrees of K+ accumulation in the narrow space of the synaptic cleft between the hair cell and the residual nerve calyx. After complete calyx removal, IK,L properties in adult animals were in fact consistent among cells and did not change during the recording. IK,L in these cells showed a quite slow deactivation kinetics (time constant ~ 1 s at –80 mV), a complex activation kinetics best described by a three exponential function, a half-activation voltage of –69 mV, and a steep voltage dependence (S = 3.68). This study provides the first complete biophysical description of the genuine properties of IK,L, and suggests that in vivo IK,L properties are dependent on K+ accumulation into the synaptic cleft. Intercellular K+ accumulation might represent a direct way to change both the hair cell and the calyx membrane potential, thus allowing an additional form of communication that cooperates with the conventional glutamatergic synaptic transmission.