Power Efficiency of Outer Hair Cell Somatic Electromotility

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Abstract
Cochlear outer hair cells (OHCs) are fast biological motors that serve to enhance the vibration of the organ of Corti and increase the sensitivity of the inner ear to sound. Exactly how OHCs produce useful mechanical power at auditory frequencies, given their intrinsic biophysical properties, has been a subject of considerable debate. To address this we formulated a mathematical model of the OHC based on first principles and analyzed the power conversion efficiency in the frequency domain. The model includes a mixture-composite constitutive model of the active lateral wall and spatially distributed electro-mechanical fields. The analysis predicts that: 1) the peak power efficiency is likely to be tuned to a specific frequency, dependent upon OHC length, and this tuning may contribute to the place principle and frequency selectivity in the cochlea; 2) the OHC power output can be detuned and attenuated by increasing the basal conductance of the cell, a parameter likely controlled by the brain via the efferent system; and 3) power output efficiency is limited by mechanical properties of the load, thus suggesting that impedance of the organ of Corti may be matched regionally to the OHC. The high power efficiency, tuning, and efferent control of outer hair cells are the direct result of biophysical properties of the cells, thus providing the physical basis for the remarkable sensitivity and selectivity of hearing. The sense of hearing is exquisitely sensitive to quiet sounds due to active mechanical amplification of sound-induced vibrations by hair cells within the inner ear. In mammals, the amplification is due to the motor action of “outer hair cells” that feed mechanical power into the cochlea. How outer hair cells are able to amplify vibrations at auditory frequencies has been somewhat of a paradox given their relatively large size and leaky electrical properties. In the present work, we examined the power conversion efficiency of outer hair cells based on first principles of physics. Results show that the motor is highly efficient over a broad range of auditory frequencies. Results also show that the motor is likely controlled by the brain in a way that allows the listener to focus attention on specific frequencies, thus improving the ability to distinguish sounds of interest in a noisy environment.