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Persistent and resurgent Na+ currents in vestibular calyx afferents.

Vestibular afferent neurons convey information from hair cells in vestibular end organs to central nuclei. These neurons can fire action potentials at high rates and firing patterns vary with the position of nerve terminal endings in neuroepithelia. Terminals contact hair cells as small bouton or large calyx endings. We investigated the biophysical properties of Na+ currents (INa) in calyx-bearing afferents. Whole cell patch clamp recordings were made from calyx terminals in thin slices of gerbil crista at different postnatal ages. A large transient Na+ current (INaT) was completely blocked by 300 nM tetrodotoxin (TTX) in mature calyces. In addition, INaT was accompanied by much smaller persistent Na+ currents (INaP) and distinctive resurgent Na+ currents (INaR), which were also blocked by TTX. ATX-II, a toxin that slows Na+ channel inactivation, enhanced INaP in immature and mature calyces. 4,9-anhydro-TTX (4,9-ah-TTX), which selectively blocks Nav1.6 channels, abolished the enhanced INa in mature, but not immature calyces. Therefore Nav1.6 channels mediate a component of INaT and INaP in mature calyces, but are minimally expressed at early postnatal days. INaR expression increased with development and in mature cristae INaR was frequently found in peripheral calyces. INaR increased the availability of Na+ channels following brief membrane depolarizations. In current clamp, the rate and regularity of action potential firing decreased in mature peripheral calyces following 4,9-ah-TTX application. Therefore Nav1.6 channels are upregulated during development, contribute to INaT, INaP and INaR and may regulate excitability by enabling higher mean discharge rates in a sub-population of mature calyx afferents.