Abstract
The hair bundle is the mechanosensory organelle of hair cells that detects mechanical stimuli caused by sounds, head motions, and fluid flows. Each hair bundle is an assembly of cellular-protrusions called stereocilia, which differ in height to form a staircase. Stereocilia have different heights, widths, and separations in different species, sensory organs, positions within an organ, hair-cell types, and even within a single hair bundle. The dimensions of the stereociliary assembly dictate how the hair bundle responds to stimuli. These hair-bundle properties have been measured previously only to a limited degree. In particular, mammalian data are either incomplete, lack control for age or position within an organ, or have artifacts owing to fixation or dehydration. Here, we provide a complete set of measurements for postnatal day (P) 11 C57BL/6J mouse apical inner hair cells (IHCs) obtained from living tissue, tissue mildly-fixed for fluorescent imaging, or tissue strongly fixed and dehydrated for scanning electronic microscopy (SEM). We found that hair bundles mildly-fixed for fluorescence had the same dimensions as living hair bundles, whereas SEM-prepared hair bundles shrank uniformly in stereociliary heights, widths, and separations. By determining the shrinkage factors, we imputed live dimensions from SEM that were too small to observe optically. Accordingly, we created the first complete blueprint of a living IHC hair bundle. We show that SEM-prepared measurements strongly affect calculations of a bundle’s mechanical properties – overestimating stereociliary deflection stiffness and underestimating the fluid coupling between stereocilia. The methods of measurement, the data, and the consequences we describe illustrate the high levels of accuracy and precision required to understand hair-bundle mechanotransduction.
Highlights
Hair bundles are the mechanosensory organelles of hair cells that detect forces induced by sound in auditory systems, head motion in vestibular systems, or fluid flow in lateral lines
Hair-bundle investigations are typically performed in the mouse from P0 to P11, when the cochlear bone can be removed with less damage to the hair cells than at older ages (Kim and Fettiplace, 2013; Asai et al, 2018; Corns et al, 2018; Trouillet et al, 2021)
To avoid the heterogeneity found within the most apical inner hair cells (IHCs), we focused on hair bundles from the 90th to 160th IHCs from the apex (Figure 1A)
Summary
Hair bundles are the mechanosensory organelles of hair cells that detect forces induced by sound in auditory systems, head motion in vestibular systems, or fluid flow in lateral lines. The hair bundle consists of an assembly of stereocilia – cylindrical cellular protrusions with a beveled top and a tapered bottom filled with F-actin (Duvall et al, 1966; Mulroy, 1974; Flock and Cheung, 1977; DeRosier et al, 1980; Tilney et al, 1980; Tilney and Saunders, 1983; Kaltenbach et al, 1994). Mechanical deflection of the hair bundle toward its tallest row extends gating springs, composed of tip links and other elements, which convey forces that modulate mechanotransducer-channel open probability, which in turn drives the hair-cell receptor potential via the influx of potassium ions into the cell (Davis, 1965; Howard and Hudspeth, 1988; Bartsch et al, 2019; Ó Maoiléidigh and Ricci, 2019)
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