Temporal resolution and temporal integration of short pulses at the auditory periphery of echolocating animals

Abstract

To explain the temporal integration and temporal resolution abilities revealed in echolocating animals by behavioral and electrophysiological experiments, the peripheral coding of sounds in the high-frequency auditory system of these animals is modeled. The stimuli are paired pulses similar to the echolocating signals of the animals. Their duration is comparable with or smaller than the time constants of the following processes: formation of the firing rate of the basilar membrane, formation of the receptor potentials of internal hair cells, and recovery of the excitability of spiral ganglion neurons. The models of auditory nerve fibers differ in spontaneous firing rate, response thresholds, and abilities to reproduce small variations of the stimulus level. The formation of the response to the second pulse of a pair of pulses in the multitude of synchronously excited high-frequency auditory nerve fibers may occur in only two ways. The first way defined as the stochastic mechanism implies the formation of the response to the second pulse as a result of the responses of the fibers that did not respond to the first pulse. This mechanism is based on the stochastic nature of the responses of auditory nerve fibers associated with the spontaneous firing rate. The second way, defined as the repeatition mechanism, implies the appearance of repeated responses in fibers that already responded to the first pulse but suffered a decrease in their response threshold after the first spike generation. This mechanism is based on the deterministic nature of the responses of fibers associated with refractoriness. The temporal resolution of pairs of short pulses, which, according to the data of behavioral experiments, is about 0.1–0.2 ms, is explained by the formation of the response to the second pulse through the stochastic mechanism. A complete recovery of the response to the second pulse, which, according to the data of electrophysiological studies of short-latency evoked brainstem potentials in dolphins, occurs within 5 ms, is explained by the formation of the response to the second pulse through the repetition mechanism. The time constant of temporal integration, which, according to the behavioral experiments at threshold levels of pulses, is about 0.2–0.3 ms, is explained by the integrating properties of internal hair cells, etc. It is shown that, at the high-frequency auditory periphery, the temporal integration imposes no limitations on the temporal resolution, because both integration and resolution are different characteristics of the same multiple response of synchronously excited fibers.