Fast Negative Feedback Enables Mammalian Auditory Nerve Fibers to Encode a Wide Dynamic Range of Sound Intensities

Mark Ospeck,Li I Zhang

doi:10.1371/journal.pone.0032384

Abstract

Mammalian auditory nerve fibers (ANF) are remarkable for being able to encode a 40 dB, or hundred fold, range of sound pressure levels into their firing rate. Most of the fibers are very sensitive and raise their quiescent spike rate by a small amount for a faint sound at auditory threshold. Then as the sound intensity is increased, they slowly increase their spike rate, with some fibers going up as high as ∼300 Hz. In this way mammals are able to combine sensitivity and wide dynamic range. They are also able to discern sounds embedded within background noise. ANF receive efferent feedback, which suggests that the fibers are readjusted according to the background noise in order to maximize the information content of their auditory spike trains. Inner hair cells activate currents in the unmyelinated distal dendrites of ANF where sound intensity is rate-coded into action potentials. We model this spike generator compartment as an attenuator that employs fast negative feedback. Input current induces rapid and proportional leak currents. This way ANF are able to have a linear frequency to input current (f-I) curve that has a wide dynamic range. The ANF spike generator remains very sensitive to threshold currents, but efferent feedback is able to lower its gain in response to noise.

Highlights

Mammals have a powerful cochlear amplifier and so are able to have very low auditory thresholds for detecting sound waves (,0 dB SPL, corresponding to micro Pascal pressure fluctuations) [1]
Model Below about 3 kHz, auditory nerve fibers (ANF) phase lock their action potentials to the sound waves sensed by their respective inner hair cell (IHC) [1]
In a myelinated axon it is typically maintained in a range from millimeters up to centimeters, with the gaps in myelination kept to less than one micron in length [6]. Inside the cochlea it seems that the ANF radii are intentionally kept low and membrane conductance high, so that the fibers maintain a short space constant calculated to be in the 100 micron range

Summary

Introduction

Mammals have a powerful cochlear amplifier and so are able to have very low auditory thresholds for detecting sound waves (,0 dB SPL, corresponding to micro Pascal pressure fluctuations) [1]. Surprisingly, they are able to distinguish variations in sound intensity at levels ,70 dB above this sensory threshold (107 fold power increase) [1,2]. Most fibers are sensitive to very faint sounds, but at the same time still respond to a wide dynamic range of sound inputs This contradiction is known as the dynamic range problem in mammalian hearing [2]. The problem is how to account for a vast range of hearing in which a very sensitive mammalian hearing apparatus is able to rate code sound intensity across a gigantic input power range

Methods

Results

Conclusion