Abstract

Hair cell mechanosensitivity resides in the sensory hair bundle, an apical protrusion of actin-filled stereocilia arranged in a staircase pattern. Hair bundle deflection activates mechano-electric transduction (MET) ion channels located near the tops of the shorter rows of stereocilia. The elicited macroscopic current is shaped by the hair bundle motion so that the mode of stimulation greatly influences the cell’s output. We present data quantifying the displacement of the whole outer hair cell bundle using high-speed imaging when stimulated with a fluid jet. We find a spatially non-uniform stimulation that results in splaying, where the hair bundle expands apart. Based on modeling, the splaying is predominantly due to fluid dynamics with a small contribution from hair bundle architecture. Additionally, in response to stimulation, the hair bundle exhibited a rapid motion followed by a slower motion in the same direction (creep) that is described by a double exponential process. The creep is consistent with originating from a linear passive system that can be modeled using two viscoelastic processes. These viscoelastic mechanisms are integral to describing the mechanics of the mammalian hair bundle.

Highlights

  • The auditory system relies on a cochlear amplification process to achieve its high dynamic range and sharp frequency selectivity

  • Mammalian cochlear hair bundles are unique in having fewer stereocilia rows, typically three, with the lower two rows possessing functional mechano-electric transduction (MET) channels (Beurg et al, 2009)

  • As hair bundles are stimulated in a variety of manners in vivo, from free standing to embedded in an overlying membrane and from sinusoidal modulation to static displacement, bundle coherence is important in shaping how these stimulations are translated to a force sensed by the MET channel

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Summary

Introduction

The auditory system relies on a cochlear amplification process to achieve its high dynamic range and sharp frequency selectivity. Hair bundle arrays in different species and organs vary in height, number of rows, stereocilia thickness, staircase step size, and coherence, defined here as how uniformly and reproducibly stereocilia will move relative to each other in time, direction and distance. Mammalian cochlear hair bundles are unique in having fewer stereocilia rows, typically three, with the lower two rows possessing functional mechano-electric transduction (MET) channels (Beurg et al, 2009). Mammalian cochlear bundles lack coherence (Langer et al, 2001; Nam et al, 2015; Scharr and Ricci, 2018) This asynchrony of stereocilia motion can alter the macroscopic manifestations of channel gating and adaptation (Nam et al, 2015). Understanding the within bundle and between stereocilia variations in movement is critical to constructing the force sensed by the MET channels which cumulatively generates the receptor current

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