Overturning the mechanisms of cochlear amplification via area deformations of the organ of Corti

Abstract

The mammalian ear embeds a cellular amplifier that boosts sound-induced hydromechanical waves as they propagate along the cochlea. The operation of this amplifier is not fully understood and is difficult to disentangle experimentally. In the prevailing view, cochlear waves are amplified by the piezo-electric action of the outer hair cells (OHCs), whose cycle-by-cycle elongations and contractions inject power into the local motion of the basilar membrane (BM). Concomitant deformations of the opposing (or “top”) side of the organ of Corti are assumed to play a minor role and are generally neglected. However, analysis of intracochlear motions obtained using optical coherence tomography calls this prevailing view into question. In particular, the analysis suggests that (i) the net local power transfer from the OHCs to the BM is either negative or highly inefficient; and (ii) vibration of the top side of the organ of Corti plays a primary role in traveling-wave amplification. A phenomenological model derived from these observations manifests realistic cochlear responses and suggests that amplification arises almost entirely from OHC-induced deformations of the top side of the organ of Corti. In effect, the model turns classic assumptions about spatial impedance relations and power-flow direction within the sensory epithelium upside down.

A Guinea Pig Model Suggests That Objective Assessment of Acoustic Hearing Preservation in Human Ears With Cochlear Implants Is Confounded by Shifts in the Spatial Origin of Acoustically Evoked Potential Measurements Along the Cochlear Length

“…10 of Salt et al 2017), a first approximation of these results may suggest that the in situ cochlear implant affects cochlear at frequency places other than the location of the implant. Traveling wave cochlear amplification, which should present in our otherwise naively implanted ears that had sensitive thresholds and produced otoacoustic emissions (Salt et al 2017), accumulates longitudinally (Dewey et al 2019; Altoè et al 2022; Guinan 2022). However, this spatial buildup of cochlear amplification occurs only near the peak region associated with the characteristic frequency place.…”

A frame and a hotspot in cochlear mechanics

“…Conversely, fluid moving to accommodate the hotspot motion may be critical to the longitudinal flow of energy towards the best place. Several recent cochlear models have explored the role of active fluid flow in frequency tuning (Altoe et al, 2022; Guinan, 2022; He et al, 2022). The findings here add to the experimental data guiding the models.…”

“…A central question of cochlear mechanics remains: how does the BM, and OCC frame in general, respond to OHC active forces only at frequencies in the BF peak, when OHC active forces are present through the full range of sub-BF frequencies? Mathematical models and concepts can replicate this phenomenon (Nankali et al, 2020; Yoon et al, 2011, deBoer and Nuttall, 2000; Altoe et al, 2022; Sisto et al, 2021; Dong and Olson, 2013) but their physiological underpinnings remain tenuous. OCT has delivered a wealth of new data regarding the coordinated responses of OHCs, supporting cells and their surrounding fluid and extracellular structures.…”

A Cochlea-Slice Model using Floquet Boundary Conditions shows Global Tuning

“…Recently, a body of theory was developed that explains traveling wave amplification by changes in OoC area (Altoè et al, 2022; Guinan, 2022) from OHCs cyclically squeezing the OoC transversely and producing fluid flow along the OoC tunnels (Guinan, 2022). Longitudinal flow of fluid in sulcus was not considered but it could also be involved insofar as squeezing the OoC expands it into the sulcus.…”