Two-Dimensional Cochlear Micromechanics Measured In Vivo Demonstrate Radial Tuning within the Mouse Organ of Corti

The exquisite sensitivity and frequency discrimination of mammalian hearing underlie the ability to understand complex speech in noise. This requires force generation by cochlear outer hair cells(OHCs) to amplify the basilar membranetraveling wave; however, it is unclear how amplification is achieved with sharp frequency tuning. Here we investigated the origin of tuning by measuring sound-induced 2-D vibrations within the mouse organof Cortiin vivo . Our goal was to determine the transfer function relating the radial shear between the structures that deflect the OHC bundle, the tectorial membraneand reticular lamina, to the transverse motion of the basilar membrane. We found that, after normalizing their responses to the vibration of the basilar membrane, the radial vibrations of the tectorial membraneand reticular lamina were tuned. The radial tuning peaked at a higher frequency than transverse basilar membranetuning in the passive, postmortem condition. The radial tuning was similar in dead mice, indicating that this reflected passive, not active, mechanics. These findings were exaggerated in TectaC1509G/C1509G mice, where the tectorial membraneis detached from OHC stereocilia, arguing that the tuning of radial vibrations within the hair cellepithelium is distinct from tectorial membranetuning. Together, these results reveal a passive, frequency-dependent contribution to cochlear filtering that is independent of basilar membranefiltering. These data argue that passive mechanics within the organof Cortisharpen frequency selectivity by defining which OHCs enhance the vibration of the basilar membrane, thereby tuning the gain of cochlear amplification. SIGNIFICANCE STATEMENT Outer hair cellsamplify the traveling wave within the mammalian cochlea. The resultant gain and frequency sharpening are necessary for speech discrimination, particularly in the presence of background noise. Here we measured the 2-D motion of the organof Cortiin mice and found that the structures that stimulate the outer hair cell stereocilia, the tectorial membraneand reticular lamina, were sharply tuned in the radial direction. Radial tuning was similar in dead mice and in mice lacking a tectorial membrane. This suggests that radial tuning comes from passive mechanics within the hair cellepithelium, and that these mechanics, at least in part, may tune the gain of cochlear amplification.