Constructing a representation of periodicity for temporal pattern recognition in a vertebrate auditory system

Abstract

The inner ear of the sound-producing fish Pollimyrus (family Mormyridae) consists of two gas-filled bubbles attached to the sacculi otolithic endorgans and shows little specialization for peripheral frequency analysis as is found in the mammalian cochlea. Therefore, questions arise regarding how sounds are represented and analyzed in the central nervous system, and specifically, how temporal pattern recognition arises at midbrain levels, where it has been observed previously. Neuronal pathway tracing reveals that the brainstem auditory pathway is organized around successive levels of processing, which include the auditory nerve, first and second order medullary nuclei, and the auditory midbrain. Physiological responses showed transformations at each successive station. Spike timing at lower levels temporally codes intervals and periods in stimuli over a remarkable range, from one second repetition rates, to 10–80 millisecond inter-click intervals, to the shortest sinusoidal periods that this animal can discriminate (i.e. \u3c1 ms). Temporal coding is extreme and appears limited only by the shortest intervals possible between action potentials. Convergence of independently generated spike trains is likely required for high frequency temporal coding. Evidence for convergence derives from intracellular recordings and from a predictive model, which motivates and is supported by new analyses of spike time data. Finally, a class of second order chopper responses is described. These generate spike trains with predictable temporal structures that are modulated across trials, but which are not correlated to the structure of the stimulus waveform. We conclude that temporal pattern recognition, in the form of narrow band spike rate tuning to stimulus periods and intervals, is an emergent property of midbrain neurons. This conclusion is based on results reported here that broadband temporal coding predominates in both primary afferents and first order medullary neurons. Second order medullary chopper responses radically depart from temporal coding. Instead, patterned spiking in these neurons codes stimulus repetition number over long durations (\u3e20 sec). All results are discussed within the neuroethological context of the communication behaviors that this anatomy and physiology must serve