The micromechanical mechanisms that underpin tuning and dynamic range compression in the mammalian inner ear are fundamental to hearing, but poorly understood. Here, we present new, high-resolution optical measurements that directly map sound-evoked vibrations on to anatomical structures in the intact, living gerbil cochlea. The largest vibrations occur in a tightly delineated hotspot centering near the interface between the Deiters' and outer hair cells. Hotspot vibrations are less sharply tuned, but more nonlinear, than basilar membrane vibrations, and behave non-monotonically (exhibiting hyper-compression) near their characteristic frequency. Amplitude and phase differences between hotspot and basilar membrane responses depend on both frequency and measurement angle, and indicate that hotspot vibrations involve longitudinal motion. We hypothesize that structural coupling between the Deiters' and outer hair cells funnels sound-evoked motion into the hotspot region, under the control of the outer hair cells, to optimize cochlear tuning and compression.