Vestibular calyx, potassium: Kalium in Calyx Regnat.

Abstract

The inner ear is noteworthy for its unusual synaptic arrangements. One particularly striking example is the extraordinary calyx synapse of vestibular afferents in amniotic vertebrates. This enlarged ending completely engulfs one or more type I hair cells, presumably for encoding aspects of vestibular sensation useful to animals with necks, but the how and why have been resistant to explanation. It is known that calyces are the terminals of larger diameter ‘irregular’ afferents that are more sensitive to higher frequencies of head motion (Goldberg, 2000; Straka et al. 2016). This provides some rationale for a specialization found in animals whose heads can move independent of the body and therefore might require higher frequency signalling. However, the dynamics of vestibular signalling are obscured by the fact that the epithelium is essentially mechanically coherent, with neighbouring hair cells stimulated similarly by the motion of an overlying cupular or otolithic membrane. Thus kinetic discrimination of vestibular signals must depend heavily on stages after the global end-organ stimulus itself. This presents an intriguing challenge for sensory and synaptic physiologists. How do cellular and synaptic mechanisms filter the generic input to better inform the central nervous system of stimulus dynamics? As technological advances have opened new avenues of study, the questions have advanced similarly. Previous intracellular calyx recordings revealed transient glutamatergic synaptic currents (quantal) common to all hair cell synapses, and non-glutamatergic steady-state (non-quantal) currents specific to the calyx. These latter non-quantal signals have been proposed to be due to a variety of mechanisms: accumulation of potassium, or protons, or direct, ephaptic polarization (Holt et al. 2007; Songer & Eatock, 2013; Highstein et al. 2014). In this issue of The Journal of Physiology, Contini et al. (2016) demonstrate that potassium (Latin: kalium) accumulation in the femtolitre (10−15) extracellular space confined by the calyx depolarizes both the presynaptic hair cell and the postsynaptic afferent, enabling more faithful transmission of quantal transmitter release. While the overall functional significance remains to be determined fully, this work lays a biophysical foundation for that ultimate explanation. The authors achieve these results by expertly employing paired recordings from type I hair cells and postsynaptic calyces (a significant technical achievement) in excised cristae of the turtle posterior semicircular canal. The accumulation of potassium in the cleft depolarizes the presynaptic hair cell into a range where voltage-dependent calcium channels have a higher open probability, and so are more likely to trigger glutamate release. Potassium accumulation also depolarizes the postsynaptic calyx, principally by flux through HCN channels, bringing the afferent closer to threshold. An additional benefit of this process is to increase membrane conductance and thereby shorten the membrane time constant – particularly important for the afferent whose branching, complex calyces present a substantial capacitative load that would otherwise slow voltage signals. How does this potassium component benefit vestibular signalling? Vestibular stimuli move overlying cupular or otolithic membranes to activate many hair cells simultaneously. The potassium-dependent depolarization of all the type I hair cells engulfed by a complex calyx will enhance the effect of their quantal release, as well as that from simultaneously activated type II hair cells presynaptic to the outer face of the calyx. These studies provide an important insight: potassium accumulation in the restricted cleft formed by the calyx may serve to tighten the temporal correlation of transmitter release and afferent firing and thereby enhance sensitivity for rapid head motions. None declared.