Aligned Organization of Synapses and Mitochondria in Auditory Hair Cells

Liu, Jing; Wang, Shengxiong; Lu, Yan; Wang, Haoyu; Wang, Fangfang; Qiu, Miaoxin; Xie, Qiwei; Han, Hua; Hua, Yunfeng

doi:10.1007/s12264-021-00801-w

Cited by 13 publications

(21 citation statements)

References 52 publications

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“…In line with this notion, an asymmetric mitochondrial distribution along the radial plane has been previously described in the mammalian IHCs (Bullen et al, 2015). Further, our SBEM quantifications of the midcochlea (Liu et al, 2022) and the 28-kHz region (this study) corroborate highly correlated spatial gradients of mitochondria and ribbons inside a subcellular domain confined to 4.5 -5 μm from the basolateral IHC pole (Fig 4B). This finding is significant since it provides a structural cue for defining the putative ribbon-associated mitochondria (RAM).…”

Section: Discussionsupporting

confidence: 90%

“…Differential Synaptopathy in the IHCs upon Noise Damage. It has been recently showed that the staggered mid-cochlea IHCs can be subdivided into two distinct morphological subtypes (Liu et al, 2022;Yin et al, 2014). In both 16 kHz-and 28 kHz-region, we confirmed (which was not certified by peer review) is the author/funder.…”

Section: Resultssupporting

confidence: 56%

“…Enlarged and Multi-ribbons after Acoustic Overexposures. Using the established image analysis pipeline powered by artificial intelligence (Liu et al, 2022), we volume reconstructed 112 intact IHCs and all 1710 basolateral pole-resided ribbon synapses in the SBEM datasets (Fig 2A and Table 1). As spatial resolution of the SBEM enabled capturing of different ribbon morphologies including multi-ribbons (Fig 2B ), we set out to characterize the exposure-related changes of the IHC ribbons.…”

Section: Resultsmentioning

confidence: 99%

“…The copyright holder for this preprint this version posted March 1, 2023. ; https://doi.org/10.1101/2023.02.27.530354 doi: bioRxiv preprint Hua et al, 2021;Liu et al, 2022;Michanski et al, 2019;Payne et al, 2021). Here, we employed serial block-face scanning electron microscopy (SBEM) to capture presynaptic structural changes in six large datasets of the cochlea, which were acquired from middle and basal turns of juvenile mice with or without acoustic overexposure history.…”

Section: Introductionmentioning

confidence: 99%

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Noise-induced synaptopathy impacts the long and short sensory hair cells differently in the mammalian cochlea

Wang

et al. 2023

Preprint

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In mammals, neural encoding of sounds is mediated by ribbon-type synapses between inner ear hair cells (IHCs) and postsynaptic spiral ganglion neurons. These specialized connections are arranged along the IHC basolateral surface with gradient changes in morphology and electrophysiological properties, which are essential for the level coding of sound intensity. Large synaptic ribbons, which predominantly reside on the modiolar IHC face, are responsive to loud sounds and more susceptible to acoustic insults. Selective loss of them is the major cause for reduced cochlear audible range. However, other than fewer ribbons after noise exposure, the consequential presynaptic reorganization in the IHCs remains less characterized. Here, by means of volume electron microscopy and artificial intelligence-assisted image analysis, we investigated noise exposure-related changes in the mouse IHCs. Apart from morphological changes of the ribbon-type active zones, our quantifications reveal differential synaptic reorganization and mitochondrial remodeling in an IHC subtype-specific manner. Together, these results argue for putative presynaptic mechanisms underlying activity-dependent structural changes of synaptic ribbons and the associated mitochondrial network (which powers the neurotransmission) in the sensory epithelial cells.

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Section: Discussionsupporting

confidence: 90%

Section: Resultssupporting

confidence: 56%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Noise-induced synaptopathy impacts the long and short sensory hair cells differently in the mammalian cochlea

Wang

et al. 2023

Preprint

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“…A recent study indicates that there are nearly 500 mitochondria found in a primate cone photoreceptor after SBFSEM reconstruction (Hayes et al, 2021). Another recent study (Liu et al, 2022) used SBFSEM to reconstruct mitochondria from mammalian cochlear hair cells, and estimated mitochondria numbered into the thousands. A better established measurement for comparison is mitochondrial volume as a fraction of the total cell volume (Posakony et al, 1977).…”

Section: Discussionmentioning

confidence: 99%

Activity regulates a cell type-specific mitochondrial phenotype in zebrafish lateral line hair cells

McQuate

Knecht

Raible

2022

Preprint

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Hair cells of the inner ear are particularly sensitive to changes in mitochondria, the subcellular organelles necessary for energy production in all eukaryotic cells. There are over thirty mitochondrial deafness genes, and mitochondria are implicated in hair cell death following noise exposure, aminoglycoside antibiotic exposure, as well as in age-related hearing loss. However, little is known about the basic aspects of hair cell mitochondrial biology. Using hair cells from the zebrafish lateral line as a model and serial block-face scanning electron microscopy, we have quantifiably characterized a unique hair cell mitochondrial phenotype that includes (1) a high mitochondrial volume, and (2) specific mitochondrial architecture: multiple small mitochondria apically, and a reticular mitochondrial network basally. This phenotype develops gradually over the lifetime of the hair cell. Disrupting this mitochondrial phenotype with a mutation in opa1 impacts mitochondrial health and function. While hair cell activity is not required for the high mitochondrial volume, it shapes the mitochondrial architecture, with mechanotransduction necessary for all patterning, and synaptic transmission necessary for development of mitochondrial networks. These results demonstrate the high degree to which hair cells regulate their mitochondria for optimal physiology, and provide new insights into mitochondrial deafness.

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Electron Microscopic Mapping of Mitochondrial Morphology in the Cochlear Nerve Fibers

Lu,

Jiang,

Wang

et al. 2024

JARO

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Aligned Organization of Synapses and Mitochondria in Auditory Hair Cells

Cited by 13 publications

References 52 publications

Noise-induced synaptopathy impacts the long and short sensory hair cells differently in the mammalian cochlea

Noise-induced synaptopathy impacts the long and short sensory hair cells differently in the mammalian cochlea

Activity regulates a cell type-specific mitochondrial phenotype in zebrafish lateral line hair cells

Electron Microscopic Mapping of Mitochondrial Morphology in the Cochlear Nerve Fibers

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