In situ motions of individual inner-hair-cell stereocilia from stapes stimulation in adult mice

Wang, Yanli; Steele, Charles R.; Puria, Sunil; Ricci, Anthony J.

doi:10.1038/s42003-021-02459-6

Cited by 33 publications

(4 citation statements)

References 60 publications

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“…Live stereociliary height measurements allow us to determine the extent to which stereociliary stiffness differs between rows owing to differences in stereociliary heights. Stereocilia pivot at their insertion point into the hair-cell’s apical surface ( Howard and Ashmore, 1986 ; Crawford et al, 1989 ; Karavitaki and Corey, 2010 ; Wang et al, 2021 ; Figure 7A ). A stereocilium’s deflection stiffness K d relative to its pivot stiffness K p is given by…”

Section: Resultsmentioning

confidence: 99%

Dimensions of a Living Cochlear Hair Bundle

Miller

Atkinson

Mendoza

et al. 2021

Front. Cell Dev. Biol.

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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.

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Section: Resultsmentioning

confidence: 99%

Dimensions of a Living Cochlear Hair Bundle

Miller

Atkinson

Mendoza

et al. 2021

Front. Cell Dev. Biol.

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“…While it remains a complex procedure, the sensitive data collected in the current study demonstrates the feasibility of this new approach. Since the gerbils have been commonly used for cochlear mechanical study, the reported method is useful not only for heterodyne low-coherence interferometry but also for optical coherence tomography and for imaging the organ of Corti in vivo 46 .…”

Section: Discussionmentioning

confidence: 99%

The reticular lamina and basilar membrane vibrations in the transverse direction in the basal turn of the living gerbil cochlea

Burwood

Porsov

et al. 2022

Sci Rep

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The prevailing theory of cochlear function states that outer hair cells amplify sound-induced vibration to improve hearing sensitivity and frequency specificity. Recent micromechanical measurements in the basal turn of gerbil cochleae through the round window have demonstrated that the reticular lamina vibration lags the basilar membrane vibration, and it is physiologically vulnerable not only at the best frequency but also at the low frequencies. These results suggest that outer hair cells from a broad cochlear region enhance hearing sensitivity through a global hydromechanical mechanism. However, the time difference between the reticular lamina and basilar membrane vibration has been thought to result from a systematic measurement error caused by the optical axis non-perpendicular to the cochlear partition. To address this concern, we measured the reticular lamina and basilar membrane vibrations in the transverse direction through an opening in the cochlear lateral wall in this study. Present results show that the phase difference between the reticular lamina and basilar membrane vibration decreases with frequency by ~ 180 degrees from low frequencies to the best frequency, consistent with those measured through the round window. Together with the round-window measurement, the low-coherence interferometry through the cochlear lateral wall demonstrates that the time difference between the reticular lamina and basilar membrane vibration results from the cochlear active processing rather than a measurement error.

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“…The boundary conditions on the basal and apical faces of the slice need to be specified. In real cochleae there is considerable motion of cochlear structures in the longitudinal direction (Karavitaki and Mountain, 2007;Wang et al, 2021), so clamping the slice faces, as was done by Zagadou et al (2020), is not realistic. Instead, we strived to capture the motion induced by the traveling wave by using a computationally-efficient "Floquet" boundary condition that mimicked how the traveling wave changed the phases of the motions at the edges of the slice.…”

Section: Wavenumber and The Floquet Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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

Tubelli

Motallebzadeh

Guinan

et al. 2022

Preprint

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A common assumption about the cochlea is that the local characteristic frequency (CF) is determined by a local resonance of basilar-membrane (BM) stiffness with the mass of the organ-of-Corti (OoC) and entrained fluid. We modeled the cochlea while avoiding such a priori assumptions by using a finite-element model of a 20-um-thick cross-sectional slice of the middle turn of a passive gerbil cochlea. The model had anatomically accurate structural details with physiologically appropriate material properties and interactions between the fluid spaces and solid OoC structures. The longitudinally-facing sides of the slice had a phase difference that mimicked the traveling-wave wavelength at the location of the slice by using Floquet boundary conditions. A paired volume-velocity drive was applied in the scalae at the top and bottom of the slice with the amplitudes adjusted to mimic experimental BM motion. The development of this computationally efficient model with detailed anatomical structures is a key innovation of this work. The resulting OoC motion was greatest in the transverse direction, stereocilia-tip deflections were greatest in the radial direction and longitudinal motion was small in OoC tissue but became large in the sulcus at high frequencies. If the source velocity and wavelength were held constant across frequency, the OoC motion was almost flat across frequency, i.e., the slice showed no local resonance. A model with the source velocity held constant and the wavelength varied realistically across frequency, produced a low-pass frequency response. These results indicate that tuning in the gerbil middle turn is not produced by a resonance due to local OoC mechanical properties, but rather is produced by the characteristics of the traveling wave, manifested in the driving pressure and wavelength.

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In situ motions of individual inner-hair-cell stereocilia from stapes stimulation in adult mice

Cited by 33 publications

References 60 publications

Dimensions of a Living Cochlear Hair Bundle

Dimensions of a Living Cochlear Hair Bundle

The reticular lamina and basilar membrane vibrations in the transverse direction in the basal turn of the living gerbil cochlea

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

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