Low somatic sodium conductance enhances action potential precision in time-coding auditory neurons

Auditory nerve fibers encode sounds in the precise timing of action potentials (APs), which is used for such computations as sound localization. Timing information is relayed through several cell types in the auditory brainstem that share an unusual property: their APs are not overshooting, suggesting that the cells have very low somatic sodium conductance (g_Na). However, it is not clear how g_Na influences temporal precision. We addressed this by comparing bushy cells (BCs) in the mouse cochlear nucleus with T-stellate cells (SCs), which do have normal overshooting APs. BCs play a central role in both relaying and refining precise timing information from the auditory nerve, whereas SCs discard precise timing information and encode the envelope of sound amplitude. Nucleated-patch recording at near physiological temperature indicated that the Na current density was 62% lower in BCs, and the voltage dependence of g_Na inactivation was 13mV hyperpolarized compared with SCs. We endowed BCs with SC-like g_Na using two-electrode dynamic clamp and found that synaptic activity at physiologically relevant rates elicited APs with significantly lower probability, through increased activation of delayed rectifier channels. In addition, for two near-simultaneous synaptic inputs, the window of coincidence detection widened significantly with increasing g_Na, indicating that refinement of temporal information by BCs is degraded by g_Na. Thus, reduced somatic g_Na appears to be an adaption for enhancing fidelity and precision in time-coding neurons.