LAUSR

Significance While the near-crystalline structure of the organ-of-Corti cytoarchitecture in the mammalian cochlea has been known for some time, its functional consequences on hearing remain to be established. The present computational-modeling studies show that individual outer hair cells (OHCs) can work together to produce high hearing sensitivity and frequency selectivity because of the overlapping asymmetrical Y-shaped structures that they form with the Deiters’ cells (DCs) and phalangeal processes (PhPs). Altering the geometry and material properties of these structures reveals that all three components have a profound effect on basilar-membrane and reticular-lamina amplification and tuning. One implication is that the DCs and PhPs are not just supporting structures, but that they must also be properly restored in emerging therapies to regenerate OHCs. The field of cochlear mechanics has been undergoing a revolution due to recent findings made possible by advancements in measurement techniques. While it has long been assumed that basilar-membrane (BM) motion is the most important determinant of sound transduction by the inner hair cells (IHCs), it turns out that other parts of the sensory epithelium closer to the IHCs, such as the reticular lamina (RL), move with significantly greater amplitude for weaker sounds. It has not been established how these findings are related to the complex cytoarchitecture of the organ of Corti between the BM and RL, which is composed of a lattice of asymmetric Y-shaped elements, each consisting of a basally slanted outer hair cell (OHC), an apically slanted phalangeal process (PhP), and a supporting Deiters’ cell (DC). Here, a computational model of the mouse cochlea supports the hypothesis that the OHC micromotors require this Y-shaped geometry for their contribution to the exquisite sensitivity and frequency selectivity of the mammalian cochlea. By varying only the OHC gain parameter, the model can reproduce measurements of BM and RL gain and tuning for a variety of input sound levels. Malformations such as reversing the orientations of the OHCs and PhPs or removing the PhPs altogether greatly reduce the effectiveness of the OHC motors. These results imply that the DCs and PhPs must be properly accounted for in emerging OHC regeneration therapies.