A ratchet mechanism for amplification in low-frequency mammalian hearing

The sensitivity and frequency selectivity of hearing result from tuned amplification by an active process in the mechanoreceptive hair cells. In most vertebrates, the active process stems from the active motility of hair bundles. The mammalian cochlea exhibits an additional form of mechanical activity termed electromotility: its outer hair cells (OHCs) change length upon electrical stimulation. The relative contributions of these two mechanisms to the active process in the mammalian inner ear is the subject of intense current debate. Here, we show that active hair-bundle motility and electromotility can together implement an efficient mechanism for amplification that functions like a ratchet: Sound-evoked forces, acting on the basilar membrane, are transmitted to the hair bundles, whereas electromotility decouples active hair-bundle forces from the basilar membrane. This unidirectional coupling can extend the hearing range well below the resonant frequency of the basilar membrane. It thereby provides a concept for low-frequency hearing that accounts for a variety of unexplained experimental observations from the cochlear apex, including the shape and phase behavior of apical tuning curves, their lack of significant nonlinearities, and the shape changes of threshold tuning curves of auditory-nerve fibers along the cochlea. The ratchet mechanism constitutes a general design principle for implementing mechanical amplification in engineering applications.