Corti fluid is a medium for outer hair cell force transmission

Abstract

The mammalian cochlea amplifies sounds selectively to improve frequency resolution. However, vibrations around the outer hair cells (OHCs) are amplified non-selectively. The mechanism of the selective or non-selective amplification is unknown. This study demonstrates that active force transmission through the extracellular fluid in the organ of Corti (Corti fluid) can explain how the cochlea achieves selective sound amplification despite the non-frequency-selective action of OHCs. Computational model simulations and experiments with excised cochleae from young gerbils of both sexes were exploited. OHC motility resulted in characteristic off-axis motion of the joint between the OHC and Deiters cell (ODJ). Incorporating the Corti fluid dynamics was critical to account for the ODJ motion due to OHC motility. The incorporation of pressure transmission through the Corti fluid resulted in three distinct frequency tuning patterns depending on sites in the organ of Corti. In the basilar membrane, the responses were amplified near the best-responding frequency (BF). In the ODJ region, the responses were amplified non-selectively. In the reticular lamina, the responses were amplified near the BF but suppressed in lower frequencies. The suppressive effect of OHCs was further examined by observing the changes in tuning curves due to local inhibition of OHC motility. The frequency response of the reticular lamina resembled neural tuning, such as the hypersensitivity of tuning-curve tails after hair cell damage. Our results demonstrate how active OHCs exploit the elastic frame and viscous fluid in the organ of Corti to amplify and suppress cochlear vibrations for better frequency selectivity.Significance Statement Active outer hair cells have been considered to selectively amplify the basilar membrane vibrations near the sound's tonotopic location. However, recent observations from different labs showed that outer hair cells' action is non-selective-it spreads over the broad span of traveling waves. These observations challenge the existing theory pegged to basilar-membrane mechanics. The motion at the joint between the outer hair cell and the Deiters (ODJ) cell holds the key to account for the non-selective action of outer hair cells. We show that the characteristic motions at the ODJ are explained coherently when Corti fluid acts as the medium for outer hair cell force transmission. Our results demonstrate how non-selective outer hair cell action produces selective neural responses.