K+ Currents in Isolated Vestibular Afferent Calyx Terminals

Vestibular hair cells transduce mechanical displacements of their hair bundles into an electrical receptor potential which modulates transmitter release and subsequent action potential firing in afferent neurons. To probe ionic mechanisms underlying sensory coding in vestibular calyces, we used the whole-cell patch-clamp technique to record action potentials and K+ currents from afferent calyx terminals isolated from the semicircular canals of Mongolian gerbils. Calyx terminals showed minimal current at the mean zero-current potential (-60 mV), but two types of outward K+ currents were identified at potentials above -50 mV. The first current was a rapidly activating and inactivating K+ current that was blocked by 4-aminopyridine (4-AP, 2.5 mM) and BDS-I (up to 250 nM). The time constant for activation of this current decreased with membrane depolarization to a minimum value of similar to 1 ms. The 4-AP-sensitive current showed steady-state inactivation with a half-inactivation of approximately -70 mV. A second, more slowly activating current (activation time constant was 8.5 +/- 0.7 ms at -8 mV) was sensitive to TEA (30 mM). The TEA-sensitive current also showed steady-state inactivation with a half-inactivation of -95.4 +/- 1.4 mV, following 500-ms duration conditioning pulses. A combination of 4-AP and TEA blocked similar to 90% of the total outward current. In current clamp, single Na+-dependent action potentials were evoked following hyperpolarization to potentials more negative than the resting potential. 4-AP application increased action potential width, whereas TEA both increased the width and greatly reduced repolarization of the action potential.