Endogenously generated spontaneous spiking activities recorded from postnatal spiral ganglion neurons in vitro

Abstract

Spontaneous spiking activities in the nervous system play an important role in the neuronal development and the coding of sensory information. Such firings could be initiated by transmitter leaked from the first-order sensory receptors or as a result of the internal operation of voltage-dependent ion channels intrinsic to the neuron. We recorded endogenously-generated spontaneous action potentials (APs) from postnatal spiral ganglion (SG) neurons of mouse in vitro. SG neurons in cultures displayed statistically stable spontaneous firings with no obvious bursting, rhythmic spiking and long silent gaps for as long as the recording configuration could be maintained. Average firing rates ranged from less than 1 to over 10 spikes/s, with most cells fired around 4 spikes/s. Interpulse interval histograms were remarkably similar to those recorded in vivo from the auditory nerve, with characteristics of a Poisson-like distribution. Resting membrane potential greatly altered the AP width and the rate of spontaneous firings. Spontaneous firing rates were also found to be controlled by the availability of the Shaw-like potassium channels. In contrast, matured SG neurons did not display any spontaneous APs, probably due to a large increase in the expression of the whole-cell potassium currents in comparison to their postnatal counterparts. This study provided the first direct evidence that postnatal SG neurons were capable of generating spontaneous APs independent of inputs from hair cells. Intracellular mechanisms for generating the spontaneous random spikes and the possible roles of such spontaneous activities in the postnatal development of SG neurons are discussed.