Neural Tuning to Sound Duration in the Inferior Colliculus of the Big Brown Bat, Eptesicus fuscus

Abstract

Neural tuning to different sound durations may be a useful filter for identification of certain sounds, especially those that are biologically important. The auditory midbrains of mammals and amphibians contain neurons that appear to be tuned to sound duration. In amphibians, neurons are tuned to durations of sound that are biologically important. The purpose of this study was to characterize responses of neurons in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus, to sounds of different durations. Our aims were to determine what percent of neurons are duration tuned and how best durations are correlated to durations of echolocation calls, and to examine response properties that may be relevant to the mechanism for duration tuning, such as latency and temporal firing pattern; we also examined frequency tuning and rate-level functions. We recorded from 136 single units in the central nucleus of the IC of unanesthetized bats. The stimuli were pure tones, frequency-modulated sweeps, and broadband noise. The criterion for duration tuning was an increase in spike count of > or = 50% at some durations compared with others. Of the total units sampled, 36% were tuned to stimulus duration. All of these units were located in the caudal half of the IC. Best duration for most units ranged from < 1 to 10 ms, but a few had best durations up to > or = 20 ms. This range is similar to the range of durations of echolocation calls used by Eptesicus. All duration-tuned neurons responded transiently. The minimum latency was always longer than the best duration. Duration-tuned units have best durations and best frequencies that match the temporal structure and frequency range of the echolocation calls. Thus the results raise the hypothesis that neurons in the IC of Eptesicus, and probably the auditory midbrain of other vertebrates, are tuned to biologically important sound durations. We suggest a model for duration tuning consisting of three components: 1) inhibitory input that is correlated with the onset of the stimulus and is sustained for the stimulus duration; 2) transient excitation that is correlated with the offset of the stimulus; and 3) transient excitation that is correlated with the onset of the stimulus but is delayed in time relative to the onset of inhibition. For the neuron to fire, the two excitatory events must coincide in time; noncoincident excitatory events are not sufficient.

Encoding the Timing of Inhibitory Inputs

“…One potential role for delayed excitation of the sort that could be provided by the DCN is the identification of sound duration. Neurons in the IC of both bats and mice can show tuning to the duration of the stimulus (Brand et al 2000;Ehrlich et al 1997), and this depends on an interaction between early inhibition and a delayed excitation in the IC (Faure et al 2003). The delays in excitation that can be provided by the long latencies of DCN pyramidal cells could also contribute to this circuit.…”

An investigation of the spatial selectivity of the duration after-effect

“…It has been proposed that duration-selective neurons are present in early sensory areas for both auditory and visual information (Heron et al, 2012). Evidence for this claim comes from single cell recording studies in different mammals that have reported duration-selective neurons in both early auditory processing areas such as inferior colliculus and the auditory midbrain (Brand, Urban, & Grothe, 2000;Casseday, Ehrlich, & Covey, 1994;Ehrlich, Casseday, & Covey, 1997;He, Hashikawa, Ojima, & Kinouchi, 1997), as well as early visual areas such as area 17 & 18 (Duysens, Schaafsma, & Orban, 1996;Eriksson, Tompa, & Roland, 2008). One can argue that an early locus for duration processing can be beneficial given that the temporal integration window of neurons is known to increase along the visual processing hierarchy (Hasson, Yang, Vallines, Heeger, & Rubin, 2008).…”

A Kalman filtering approach to the representation of kinematic quantities by the hippocampal-entorhinal complex

“…We would expect to find that different notes in the composition would be represented by different cells, just as in the spatial case. It is known already that cell in the inferior colliculus of the bat and ferret show time-interval tuning (Ehrlich et al 1997); if the HEC serves a global memory role we should expect temporal tuning there as well.…”

“…''Armreaching'' neurons in the parietal cortex of primates have been used to study how visual cues are transformed from eye coordinates to arm coordinates (Ferraina et al 1997). The inferior colliculus of the bat and ferret has been used as a model for time-interval coding (Ehrlich et al 1997). The hippocampal-entorhinal complex (HEC) and its neighboring regions, in particular, contain a rich array of cells tuned to kinematic variables.…”