Sharp temporal tuning in the bat auditory midbrain overcomes spectral-temporal trade-off imposed by cochlear mechanics.

Silvio Macías,Manfred Kössl,Julio C Hechavarría

doi:10.1038/srep29129

Abstract

In the cochlea of the mustached bat, cochlear resonance produces extremely sharp frequency tuning to the dominant frequency of the echolocation calls, around 61 kHz. Such high frequency resolution in the cochlea is accomplished at the expense of losing temporal resolution because of cochlear ringing, an effect that is observable not only in the cochlea but also in the cochlear nucleus. In the midbrain, the duration of sounds is thought to be analyzed by duration-tuned neurons, which are selective to both stimulus duration and frequency. We recorded from 57 DTNs in the auditory midbrain of the mustached bat to assess if a spectral-temporal trade-off is present. Such spectral-temporal trade-off is known to occur as sharp tuning in the frequency domain which results in poorer resolution in the time domain, and vice versa. We found that a specialized sub-population of midbrain DTNs tuned to the bat’s mechanical cochlear resonance frequency escape the cochlear spectral-temporal trade-off. We also show evidence that points towards an underlying neuronal inhibition that appears to be specific only at the resonance frequency.

Highlights

Temporal information extracted from sounds by the auditory system is crucial for a wide range of behaviors including communication, prey detection, and predator avoidance
We studied the temporal characteristics of the response of RF-units to the constant frequency component of bats emissions broadcasted in the resting state and to the cochlear resonance frequency measured with distortion product otoacoustic emissions (DPOAEs)
A subpopulation of duration-tuned neurons (DTNs) (RF-DTNs) in the IC of the mustached bat are able to encode sound properties with high resolution in both the frequency and the time domain and the absence of a spectral-temporal trade-off for duration selectivity offers an excellent example of this ability

Summary

Introduction

Temporal information extracted from sounds by the auditory system is crucial for a wide range of behaviors including communication, prey detection, and predator avoidance. According to the models that explain the central implementation of duration tuning, precise sound offset encoding is instrumental for the formation of sharp duration tuning at the level of the midbrain[11]. To test the aforementioned hypothesis, we recorded from neurons that were sharply tuned to frequency while at the same time being tuned to sound duration Since these neurons first appear at the level of the midbrain, where duration tuning is computationally implemented[12], we focused on this auditory station. This species was chosen because of its interesting flutter-detection echolocation and Doppler-shift compensation behavior. The dominant frequency of the outgoing echolocation calls for a stationary (e.g. roosting) mustached bat is called its resting frequency; flying mustached bats adjust the frequencies of their calls so that the returning (and Doppler-shifted) echoes always fall within the cochlea’s region of highest sensitivity and frequency resolution

Methods

Results

Conclusion