The outer-hair-cell RC time constant: A feature, not a bug, of the mammalian cochlea

Abstract

The cochlea of the mammalian inner ear includes an active, hydromechanical amplifier thought to arise via the piezoelectric action of the outer hair cells (OHCs). A classic problem of cochlear biophysics is that the long resistance-capacitance (RC) time constant of the hair-cell membrane produces an effective cut-off frequency much lower than that of most audible sounds. The long RC time constant implies that the OHC receptor potential—and hence its electromotile response—decreases by several orders of magnitude over the frequency range of hearing. This 'RC problem' is often invoked to question the role of cycle-by-cycle OHC-based amplification in mammalian hearing. Here, we use published data and simple physical reasoning to show that the RC problem is, in practice, a relatively minor physical issue whose importance has been unduly magnified by viewing it through the wrong lens. Indeed, our analysis indicates that the long RC time constant is actually beneficial for hearing, reducing noise and distortion while increasing the fidelity of cochlear amplification.

Analysis of outer hair cell electromechanics reveals power delivery at the upper-frequency limits of hearing

“…The extent to which high frequency power conversion draws directly from voltage-driven conformational changes in prestin versus some other mechanism is not addressed. Nevertheless, the analysis shows electro-mechanical power conversion is maximized only when voltage, current, force and velocity occur at specific phases relative to each other-requirements likely met by setting the mechano-electrical transduction current, RC corner frequency, cell stiffness, and level of prestin expression along the tonotopic map in the cochlea [37][38][39]. Electrical properties of the organ of Corti are also implicated as important in power conversion, through the influence of the electro-anatomy on frequency-dependent extracellular potentials and OHC transmembrane voltage [40].…”

Outer hair cell electro-mechanical power conversion

“…The present report only analyzed data collected under voltage-clamp commands. Nevertheless, the above analysis shows electro-mechanical power conversion is maximized only when voltage, current, force and velocity occur at specific phases relative to each other --requirements likely met by setting the mechano-electrical transduction current, RC corner frequency, cell stiffness, and level of prestin expression along the tonotopic map in the cochlea [29,[32][33][34]. Electrical properties of the Corti are also implicated as important in power conversion, through the influence of the electro-anatomy on frequency-dependent extracellular potentials and OHC transmembrane voltage [35].…”