Chronic ultrastructural changes in acoustic trauma: Serial-section reconstruction of stereocilia and cuticular plates

doi:10.1016/0378-5955(87)90036-0

Hearing Research

Volume 26, Issue 1, 1987, Pages 65-88

https://doi.org/10.1016/0378-5955(87)90036-0 Get rights and content

Abstract

Two cochleas with permanent, noise-induced threshold shifts of 40 to 60 dB (as measured by responses of single, auditory-nerve fibers) were analyzed in detail, first at the light-microscopic level and subsequently with transmission electron microscopy of serial sections. The light-microscopic analysis showed that there was little hair cell loss, but widespread damage to the stereocilia, especially those on the inner hair cells and first-row outer hair cells. Transmission electron microscopy revealed no pathology in any cells or organelles in the organ of Corti except for the stereocilia and their rootlets. Stereocilia tufts on first-row OHCs and IHCs were badly damaged; those on second- and third-row OHCs appeared ultrastructurally normal. Within the IHC tuft, the damage to the tall, outer row of stereocilia was often selective: the shorter rows could remain ultrastructurally normal even when the tall row was completely missing. The data suggested that most of the structures which appear normal in a careful light-microscopic analysis are also normal at the ultrastructural level. This strengthens earlier suggestions that the correlations between light-microscopic stereocilia changes and alterations in single-unit physiology are causal in nature. The most common stereocilia pathologies were fracture, attenuation or complete loss of the stereociliary rootlets, especially in the region of the cuticular plate near the endolymphatic surface of the cell. The degree and extent of these changes were well correlated with the degree and extent of stereocilia disarray. Abnormalities of the actin-filament matrix within the stereocilia were extremely rare in unfused stereocilia, however, they were common when the stereocilia were part of a fusion bundle. Fusion of stereocilia was always associated with ectopic supracuticular cytoplasm. Based on the ultrastructural observations, different sequences of structural changes preceding the generation of disarray, loss or fusion of stereocilia are suggested.

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Inner ear hair cells assemble mechanosensitive hair bundles on their apical surface that transduce sounds and accelerations. Each hair bundle is comprised of ∼ 100 individual stereocilia that are arranged into rows of increasing height and width; their specific and precise architecture being necessary for mechanoelectrical transduction (MET). The actin cytoskeleton is fundamental to establishing this architecture, not only by forming the structural scaffold shaping each stereocilium, but also by composing rootlets and the cuticular plate that together provide a stable foundation supporting each stereocilium. In concert with the actin cytoskeleton, a large assortment of actin-binding proteins (ABPs) function to cross-link actin filaments into specific topologies, as well as control actin filament growth, severing, and capping. These processes are individually critical for sensory transduction and are all disrupted in hereditary forms of human hearing loss. In this review, we provide an overview of actin-based structures in the hair bundle and the molecules contributing to their assembly and functional properties. We also highlight recent advances in mechanisms driving stereocilia elongation and how these processes are tuned by MET.
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Noise is a common occupational and environmental hazard; however, little is known about the use of computational tools to quantitively analyze data on basilar membrane (BM) damage in noise-induced hearing loss (NIHL). Here, we established a comprehensive three-dimensional finite-element human ear model to quantify the impact of noise exposure on BM and perilymph fluid.
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This study would inform our understanding of NIHL associated with occupational noise exposure. We present a FE modelling and describe how it might provide a unique way to unravel mechanisms that drive NIHL due to loud noises.
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There was no evidence of postmortem artifact related to the fusion, loss or disarray that we are capturing here with our algorithm. Another animal study evaluated the effects of hypoxia on cochlear morphology (Shirane and Harrison, 1987) and noted “blebbing” of the apical surface, where a membrane blister forms by extrusion of cytoplasm through the hole in the actin matrix of the cuticular plate where the kinocilium was located during development (Liberman, 1987). We never saw such cytoplasmic blisters, but it is possible that they do not contain myosin 7a or espin and are thus invisible in our confocal images.
Age-related hearing loss in humans is characterized by progressive loss of threshold sensitivity, especially at high frequencies. A multivariable regression of histopathological metrics from normal-aging human cochleae (Wu et al., 2020) showed that hair cell loss better predicts the audiometric shifts than either neural loss or strial atrophy, however considerable variability in age-related threshold elevation remained unexplained. Here, we develop and apply an algorithm to quantify stereocilia pathology in high-power confocal images of inner and outer hair cells in normal aging human cochleae, aged 21 – 71 yrs. Microdissected epithelial wholemounts of the cochleae were immunostained for myosin VIIa and espin to show cuticular plates and stereocilia, respectively, and each cochlea was imaged at 10 log-spaced locations along the cochlear spiral. An approach based on Fourier transforms was used to quantify the regularity of each stereocilia bundle, and the outcome was compared to a parallel analysis by a human observer. Results show a significant age-related decline in stereocilia regularity and increase in stereocilia loss and fusion. Stereocilia pathology was especially severe on the outer hair cells and in the basal half of the cochlea, and may represent a key contributor to age-related threshold elevations. For the one case with an associated pre-mortem audiogram, the threshold shifts are better predicted from the pattern of stereocilia damage than from the pattern of hair cell loss alone.
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For example, organ of Corti morphology was investigated in excitotoxicity and deafness models or upon aging (Kudo et al., 2003; Mahendrasingam et al., 2011; Puel et al., 1998, 1995) and hair cell and supporting cell structural changes were determined upon developmental maturation or functional impairment in different species, including various rodents and bats (Daudet et al., 1998; Hayashi et al., 2007; Lenoir and Pujol, 1984; Taylor et al., 2012; Vater et al., 1997). On subcellular level, ribbon synapses were investigated to characterize their morphological differences within hair cells (Kantardzhieva et al., 2013), in mutants that lack presynaptic key proteins such as RIBEYE (Jean et al., 2018), otoferlin (Pangrsic et al., 2010; Roux et al., 2006; Vogl et al., 2015), or myosin VI (Roux et al., 2009) as well as upon maturation/aging (Michanski et al., 2019; Sobkowicz et al., 1986) and noise trauma (Liberman, 1987). Next to TEM, scanning electron microscopy (SEM) was found to be an essential tool to investigate whole cochlear structure (Chen et al., 2014; Kaltenbach and Falzarano, 1994).
The mammalian cochlea is a snail-shaped structure deeply that is embedded in the temporal bone and harbors the auditory sensory epithelium – the organ of Corti. Since the discovery of this remarkable hearing organ in the middle of the 19th century, generations of anatomists and physiologists have been attracted to study the structural and functional details of this intricate and delicate structure and thereby contributed to establishing our current understanding of peripheral sound encoding. Since these early days, the continued development of novel imaging technologies – both on light and electron microscopic level – has driven the auditory research field and now enables the visualization of cochlear structures across multiple scales with unprecedented clarity and exquisite detail. To honor these achievements, this review aims to provide a concise overview of current multi-scale imaging methodologies to investigate cochlear anatomy and cellular function in the peripheral auditory pathway. For this purpose, we will outline the technological concepts underlying these techniques – ranging from label-free to label-containing approaches – highlight their respective strengths and limitations and provide specific examples of their use in modern auditory research. We will focus on traditional as well as less conventional imaging techniques that present essential tools for unraveling the protein composition, nanoscale assembly, and physiology of the first auditory synapse and associated structures. In addition, we will introduce novel non-invasive large-scale methodologies that allow for high-resolution in situ imaging of the structurally-unperturbed cochlea and point out potential future applications. In combination, these techniques allow for a comprehensive multi-scale analysis of cochlear structure and function.
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Following the TTS-inducing noise exposure, only minor changes were observed in the stereocilia core, including a shortening of stereocilia rootlets [36]. After PTS-inducing noise trauma, more severe damage was observed in the rootlets, along with stereocilia fusion, and holes in the stereocilia actin matrix [35]. Until recently, stereocilia F-actin cores were thought to turn over through treadmilling within 48–72 h, similar to, although somewhat slower than, filopodia and microvilli [38–40].
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Chronic ultrastructural changes in acoustic trauma: Serial-section reconstruction of stereocilia and cuticular plates

Abstract

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Discharge Patterns of Single Fibers in the Cat's Auditory Nerve

Auditory-nerve activity in cats with normal and abnormal cochleas