Mechanotransduction in mammalian sensory hair cells

Abstract

In the inner ear, the auditory and vestibular systems detect and translate sensory information regarding sound and balance. The sensory cells that transform mechanical input into an electrical signal in these systems are called hair cells. A specialized organelle on the apical surface of hair cells called the hair bundle detects mechanical signals. Displacement of the hair bundle causes mechanotransduction channels to open. The morphology and organization of the hair bundle, as well as the properties and characteristics of the mechanotransduction process, differ between the different hair cell types in the auditory and vestibular systems. These differences likely contribute to maximizing the transduction of specific signals in each system. This review will discuss the molecules essential for mechanotransduction and the properties of the mechanotransduction process, focusing our attention on recent data and differences between the auditory and vestibular systems.

Keywords: Adaptation; Auditory; Cochlea; Frequency selectivity; Hair bundle; Hair cell; MET; MT; Mechanotransduction; Otolith; Stereocilia; Vestibular.

Figure 1.

(A) Depiction of an auditory outer hair cell (OHC) and a vestibular hair cell (VHC). The actin-filled stereocilia hair bundles protrude from the hair cell’s apical surface. Vestibular hair cells also possess a kinocilium (green), a tubulin-based cilium, whereas, in auditory hair cells, the kinocilium disappears during development. (B) Taking a slice through the stereocilia rows depicts the mechanotransduction process. Tension within the tip link upon stereocilia deflection causes the opening of MET channels and the influx of potassium and calcium ions into Stereocilia.

Figure 2.

Hair bundle and mechanotransduction properties that vary tonotopically in OHCs. Stereocilia length (Garfinkle and Saunders, 1983; Kaltenbach et al., 1994). Stereocilia number (Garfinkle and Saunders, 1983; Lim, 1986). Bundle shape angle (Lim, 1986). Stereocilia stiffness (Tobin et al., 2019). Gating spring stiffness (Tobin et al., 2019). MET resting tension (Tobin et al., 2019). Maximum MET current (Kim and Fettiplace, 2013). Single channel conductance (Beurg et al., 2018; Beurg et al., 2006). Calcium permeability (Kim and Fettiplace, 2013). Fast adaptation tau (Ricci et al., 2005; Waguespack et al., 2007).

Figure 3.

Activation curves in IHCs and vestibular hair cells are significantly wider than those of OHCs. (A) Example of a family of curves (bottom) in mouse cochlear hair cells (OHC-red and IHC-blue) and a mouse utricular type II hair cell (black) taken using a fluid-jet stimulus (M) and extracting the displacement of the hair bundle (middle) using high-speed imaging to generate the activation curves (Caprara et al., 2020). (B) Activation curves for multiple different cells in the same recording configuration across different cell types. Cells were recorded using an intracellular solution containing 0.1 mM BAPTA. n = 10 OHCs, P7-P9; n = 11 IHCs, P7-P8; n = 12 vestibular type II hair cells, P8-P11. (C) Summary plots of the width, resting open probability and maximum mechanotransduction current amplitude indicate a significantly lower peak current, wider activation curve, and lower resting probability in IHCs and vestibular hair cells. **** p < 0.0001 ** p < 0.01 Student’s t-test.