The cochlear outer hair cell speed paradox

Abstract

Cochlear outer hair cells (OHCs) are among the fastest known biological motors and are essential for high-frequency hearing in mammals. It is commonly hypothesized that OHCs amplify vibrations in the cochlea through cycle-by-cycle changes in length, but recent data suggest OHCs are low-pass filtered and unable to follow high-frequency signals. The fact that OHCs are required for high-frequency hearing but appear to be throttled by slow electromotility is the "OHC speed paradox." The present report resolves this paradox and reveals origins of ultrafast OHC function and power output in the context of the cochlear load. Results demonstrate that the speed of electromotility reflects how fast the cell can extend against the load, and does not reflect the intrinsic speed of the motor element itself or the nearly instantaneous speed at which the coulomb force is transmitted. OHC power output at auditory frequencies is revealed by emergence of an imaginary nonlinear capacitance reflecting the phase of electrical charge displacement required for the motor to overcome the viscous cochlear load.