The outer hair cell, one of the two mechanoreceptor cells in the cochlea, is a critical element for the frequency specificity and wide dynamic range of the mammalian ear. It has been widely assumed that the motility of this cell is responsible for these functions. Because this cell can respond to mechanical stimuli by creating force, it can modulate vibrations in the inner ear. We have been testing our hypothesis called the ``area motor model'' that proposes that the hair cell motor has an electric charge that is transferable across the membrane. This charge transfer is coupled with changes in the area of the membrane motor. Such a mechanism resembles piezoelectricity in directly converting electrical into mechanical energy. We found that this model is equivalent to a special class of piezoelectricity, one in which a small number of states produces prominent nonlinearities. If the motile mechanism is indeed piezoelectric, then mechanical energy must be converted into electrical energy reciprocally. To test the validity of this prediction, we measured charge transfer elicited by mechanical force and displacement. We found that the maximum charge transfer is 10 fC per micrometer and 200 fC/nN. By comparing these values with force production and displacement per voltage change, we found that the reciprocal relationship characteristic of piezoelectricity is satisfied. We further found that the piezoelectric coefficient of 200 fC/nN is extremely large, more than ten thousand times greater than the best piezoelectric material. Our model also predicts that cell stiffness is voltage dependent in a manner similar to the ``gating compliance'' in sensory hair bundles. The amplitude of the voltage-driven length changes should not increase with increased internal pressure, unlike stiffness-driven length changes. We experimentally tested this prediction and found that the amplitude of voltage driven length changes is indeed independent of positive pressures applied to the cell, confirming the validity of our model. These studies show that the outer hair cell is very effective in exerting force for voltage oscillations. We are currently studying whether voltage oscillations are supported at the high frequencies at which this cell operates. These efforts should identify physical principles involved in the ear and further clarify the biological role of outer hair cells.
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