Refractoriness enhances temporal coding by auditory nerve fibers

A universal property of spiking neurons is refractoriness, a transient decrease in discharge probability immediately following an action potential (spike). The refractory period lasts only one to a few milliseconds, but has the potential to affect temporal coding of acoustic stimuli by auditory neurons, which are capable of submillisecond spike-time precision. Here this possibility was investigated systematically by recording spike times from chicken auditory nerve fibers in vivo while stimulating with repeated pure tones at characteristic frequency. Refractory periods were tightly distributed, with a mean of 1.58 ms. A statistical model was developed to recapitulate each fiber's responses and then used to predict the effect of removing the refractory period on a cell-by-cell basis for two largely independent facets of temporal coding: faithful entrainment of interspike intervals to the stimulus frequency and precise synchronization of spike times to the stimulus phase. The ratio of the refractory period to the stimulus period predicted the impact of refractoriness on entrainment and synchronization. For ratios less than ∼0.9, refractoriness enhanced entrainment and this enhancement was often accompanied by an increase in spike-time precision. At higher ratios, little or no change in entrainment or synchronization was observed. Given the tight distribution of refractory periods, the ability of refractoriness to improve temporal coding is restricted to neurons responding to low-frequency stimuli. Enhanced encoding of low frequencies likely affects sound localization and pitch perception in the auditory system, as well as perception in nonauditory sensory modalities, because all spiking neurons exhibit refractoriness.