In Vivo Outer Hair Cell Length Changes Expose the Active Process in the Cochlea

Dingjun Zha,Anders Fridberger,Alfred L Nuttall,Ruikang K Wang,Sripriya Ramamoorthy,Steven L Jacques,Niloy Choudhury,Fangyi Chen

doi:10.1371/journal.pone.0032757

Abstract

BackgroundMammalian hearing is refined by amplification of the sound-evoked vibration of the cochlear partition. This amplification is at least partly due to forces produced by protein motors residing in the cylindrical body of the outer hair cell. To transmit power to the cochlear partition, it is required that the outer hair cells dynamically change their length, in addition to generating force. These length changes, which have not previously been measured in vivo, must be correctly timed with the acoustic stimulus to produce amplification.Methodology/Principal FindingsUsing in vivo optical coherence tomography, we demonstrate that outer hair cells in living guinea pigs have length changes with unexpected timing and magnitudes that depend on the stimulus level in the sensitive cochlea.Conclusions/SignificanceThe level-dependent length change is a necessary condition for directly validating that power is expended by the active process presumed to underlie normal hearing.

Highlights

The remarkable sensitivity and frequency resolution of mammalian hearing organs [1,2,3,4,5] stems from the fast motility of outer hair cells (OHCs) [6,7,8]
This process has been observed in vitro in isolated OHCs [6,12] and in situ in the low-frequency regions of cochlear explants [7] and recently published measurements suggest that length changes occur in vivo [13].To be effective in augmenting sound-evoked vibrations in vivo, the length changes must be correctly synchronized to the acoustic stimulus
We show that OHCs length changes exist in the sensitive cochlea, that these length changes depend on the sound stimulus level, and that the polarity of the length change differs from accepted theory

Summary

Introduction

The remarkable sensitivity and frequency resolution of mammalian hearing organs [1,2,3,4,5] stems from the fast motility of outer hair cells (OHCs) [6,7,8]. The central element of this process are the OHCs, which are capable of electrical-to-mechanical transduction, e.g. alterations in their membrane potential, induced by the gating of mechanically sensitive ion channels, leading to changes in cell length [6,11] This process has been observed in vitro in isolated OHCs [6,12] and in situ in the low-frequency regions of cochlear explants [7] and recently published measurements suggest that length changes occur in vivo [13].To be effective in augmenting sound-evoked vibrations in vivo, the length changes must be correctly synchronized to the acoustic stimulus. These length changes, which have not previously been measured in vivo, must be correctly timed with the acoustic stimulus to produce amplification

Methods

Results

Conclusion