A Parametric Blueprint for Optimum Cochlear Outer Hair Cell Design

The present work examines the hypothesis that cochlear outer hair cell (OHC) length, membrane properties, and mechano-electrical transduction (MET) current vary in precise proportions along the cochlear tonotopic map to optimize electro-mechanical power conversion at each characteristic frequency (CF). We tested this hypothesis in a minimal model of OHC electro-mechanics that accounts for OHC biophysical properties as well as the cochlear mechanical load. Results identify three nondimensional ratios that maximize power conversion: the ratio of the resistive-capacitive (RC) corner frequency to CF, the ratio of nonlinear to linear capacitance, and the ratio of OHC stiffness to cochlear load stiffness. Optimum efficiency requires all three ratios to be universal constants quantitatively related to each other, independent of CF and species. From a dynamical systems perspective, the same three ratios are cardinal control parameters that combine to maximize power output by poising the OHC to operate on the edge of a dynamic instability, the critical point. Results support the hypothesis that OHC properties in extant species evolved to optimize electro-mechanical power conversion. Identification of the RC corner frequency as a dynamical control parameter that sets the critical point reveals a powerful mechanism used by medial olivocochlear efferent system to exert control over OHC stability and power output. Results further suggest the upper frequency limit of mammalian hearing is not constrained by the RC corner frequency or the speed of the motor, but instead is likely limited by the size of the nucleus and membrane surface area available for protein expression. Significance Statement Results provide strong evidence that evolutionary development of OHCs was driven by pressure to enhance electro-mechanical power conversion. Efficient power conversion requires specific OHCs properties that simultaneously match the cochlear load and poise the cell at the critical point. Results identify a parametric blueprint for optimum OHC design, which we posit applies across species and CFs. The blueprint reveals biophysical principles used by OHCs to amplify vibration across the entire bandwidth of mammalian hearing, including frequencies far exceeding what might be expected based on the low pass features of the membrane-motor complex measured in isolation. When applied to short OHCs of the odontocete cetaceans for example, the blueprint predicts peak power output at frequencies exceeding 100 kHz.