Thermodynamic Signatures of Sensing and Amplification by Periodically Driven Hair-Cell Bundles

Hair cells actively drive oscillations of their mechanosensitive organelles—the hair bundles that enable hearing and balance sensing in vertebrates. Why and how some hair cells expend energy by sustaining this oscillatory motion in order to fulfill their function as sensors and amplifiers remains unknown. Here, we develop a stochastic thermodynamic theory to describe flows of energy in a periodically driven hair bundle. Our analysis of thermodynamic fluxes associated with hair-bundle motion and external sinusoidal stimulus reveals that these organelles function as thermodynamic work-to-work machines under different operational modes. One mode allows the cell to harvest energy of the external signal, whereas another channels the power supplied by the cell into the signal. These two regimes might represent thermodynamic signatures of signal sensing and amplification, respectively, which we further connect to the receptor currents through ion channels controlled by the hair bundles. In addition to energy harvesting and work transduction, our model also substantiates the capability of hair cells to operate as heaters and, at the expense of external driving, as active feedback refrigerators. We quantify the performance and robustness of the mechanical work-to-work conversion by hair bundles, whose thermodynamic efficiency in some conditions exceeds 80% of the applied power.