Action potentials and underlying voltage-dependent currents studied in cultured spiral ganglion neurons of the postnatal gerbil

Abstract

The excitability of cultured spiral ganglion (SG) neurons from early postnatal gerbil (P0–P1) was examined with the whole-cell patch-clamp technique. The role of voltage-gated currents in shaping the kinetics of action potentials (APs) was analyzed. Cultured SG neurons displayed spontaneous APs with a low rate (<0.1 Hz). The kinetics of APs were studied by injecting neurons with current pulses of various frequencies and duration. A single depolarizing pulse of long duration elicited only one AP in most SG neurons. When excited by a train of short current pulses given at rates greater than 50 Hz, the firing pattern displayed an adaptive mechanism with the result that successive APs fired with lower amplitude, broader duration and delayed peak time. Pulse trains of higher frequencies had higher failure rates in initiating APs. Current pulses given at 20 Hz or lower elicited APs that had very similar amplitudes. However, the width of the APs gradually broadened. Duration of APs was also found to be affected by the membrane potential of neurons. Between −75 mV and −55 mV, AP duration was broadened at a rate of about 33% per 10 mV depolarization. Voltage-gated currents that underlie the generation of APs were examined under voltage-clamp conditions. Tetrodotoxin-sensitive sodium currents and dihydropyridine-sensitive L-type calcium currents were found. More importantly, inactivation properties of the potassium current provided a direct explanation for the cumulative broadening of APs. This work demonstrated that SG neurons were able to fire APs long before hearing commences in gerbil. Possible roles of spontaneous APs in the development of the cochlea and the role of voltage-gated currents in the function of SG neurons under normal and pathological conditions are discussed.