Vibration hotspots reveal longitudinal funneling of sound-evoked motion in the mammalian cochlea

Abstract

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.

Organ of Corti vibration within the intact gerbil cochlea measured by volumetric optical coherence tomography and vibrometry

“…In turn 1, the compressive cochlear gain of OoC presented in a broader region more than a half octave below the BF at moderate stimuli intensities and more than one octave at high sound pressure level, i.e., 70 -80 dB SPL. This finding was consistent with the new data found in the mouse and gerbil reticular lamina and the BM vibrations (Cooper et al 2018;He et al 2018;Lee et al 2016;Ren et al 2016). This was likely because our measurements came from within the OoC near the top of the OHCs, the reticular lamina.…”

“…This nonlinear cochlear gain between 40 and 80 dB SPL was~23 dB at the BF. However, nonlinear gain was also found at frequencies down to 5 kHz with higher intensities, i.e., 70 -80 dB SPL, which was consistent with observations at the reticular lamina in the mouse and gerbil (Cooper et al 2018;He et al 2018;Lee et al 2016;Ren et al 2016). Finally, the phase demonstrated progressive lags with increasing frequency, which is consistent with traveling wave propagation.…”

“…In addition, these measurements are closer to the reticular lamina than to the BM. Previous studies have demonstrated that these two structures have subtle differences in their vibratory patterns (Cooper et al 2018;He et al 2018;Lee et al 2016;Ren et al 2016).…”

Kinetic Membrane Model of Outer Hair Cells

“…The membrane model confirms the main predictions of the 1D model: A single mode of vibration of organ of Corti can be supported up to about 10 kHz but to cover the entire auditory range cannot be supported without multiple modes of motion in the cochlear partition [13]. This prediction appears consistent with recent observations with optical techniques in that the organ of Corti shows multiple modes of motion [44][45][46].…”

A novel theoretical framework reveals more than one voltage-sensing pathway in the lateral membrane of outer hair cells

“…This association reveals that there is more than one hyperpolarized state of the prestin sensor in the lateral membrane. Also relevant biologically is the speed of the conformational change of prestin, especially given the recent proposition that OHCs' electromotility may not be the only process responsible for amplifying sound in vivo (Cooper et al, 2018;Vavakou et al, 2019). Conventional models predict that the conformational change should proceed at reaction rates ≥70-90 kHz (time constant ≤2 μs at 37°C) to not limit hearing, while considering that nonecholocating mammals exhibit a median limit of 52 kHz, with a maximum limit of 70-90 kHz for mice (Heffner et al, 2001).…”