Spatial patterns of noise-induced inner hair cell ribbon loss in the mouse mid-cochlea

Summary: In the mammalian cochlea, moderate acoustic overexposure leads to loss of ribbon-type synapse between the inner hair cell (IHC) and its postsynaptic spiral ganglion neuron (SGN), causing a reduced dynamic range of hearing but not a permanent threshold elevation. A prevailing view is that su...

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Main Authors: Yan Lu, Jing Liu, Bei Li, Haoyu Wang, Fangfang Wang, Shengxiong Wang, Hao Wu, Hua Han, Yunfeng Hua
Format: Article
Language:English
Published: Elsevier 2024-02-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004224000464
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author Yan Lu
Jing Liu
Bei Li
Haoyu Wang
Fangfang Wang
Shengxiong Wang
Hao Wu
Hua Han
Yunfeng Hua
author_facet Yan Lu
Jing Liu
Bei Li
Haoyu Wang
Fangfang Wang
Shengxiong Wang
Hao Wu
Hua Han
Yunfeng Hua
author_sort Yan Lu
collection DOAJ
description Summary: In the mammalian cochlea, moderate acoustic overexposure leads to loss of ribbon-type synapse between the inner hair cell (IHC) and its postsynaptic spiral ganglion neuron (SGN), causing a reduced dynamic range of hearing but not a permanent threshold elevation. A prevailing view is that such ribbon loss (known as synaptopathy) selectively impacts the low-spontaneous-rate and high-threshold SGN fibers contacting predominantly the modiolar IHC face. However, the spatial pattern of synaptopathy remains scarcely characterized in the most sensitive mid-cochlear region, where two morphological subtypes of IHC with distinct ribbon size gradients coexist. Here, we used volume electron microscopy to investigate noise exposure-related changes in the mouse IHCs with and without ribbon loss. Our quantifications reveal that IHC subtypes differ in the worst-hit area of synaptopathy. Moreover, we show relative enrichment of mitochondria in the surviving SGN terminals, providing key experimental evidence for the long-proposed role of SGN-terminal mitochondria in synaptic vulnerability.
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spelling doaj.art-8fd321a7350348f1abc42bf22c6b855b2024-01-24T05:21:42ZengElsevieriScience2589-00422024-02-01272108825Spatial patterns of noise-induced inner hair cell ribbon loss in the mouse mid-cochleaYan Lu0Jing Liu1Bei Li2Haoyu Wang3Fangfang Wang4Shengxiong Wang5Hao Wu6Hua Han7Yunfeng Hua8Department of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People’s Hospital, Shanghai 200125, China; Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai 200125, China; Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases, Shanghai 200125, China; Shanghai Institute of Precision Medicine, Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200125, ChinaLaboratory of Brain Atlas and Brain-inspired Intelligence, Institute of Automation, Chinese Academy of Sciences, Beijing 100190, ChinaDepartment of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People’s Hospital, Shanghai 200125, China; Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai 200125, China; Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases, Shanghai 200125, ChinaShanghai Institute of Precision Medicine, Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200125, ChinaShanghai Institute of Precision Medicine, Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200125, ChinaShanghai Institute of Precision Medicine, Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200125, ChinaDepartment of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People’s Hospital, Shanghai 200125, China; Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai 200125, China; Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases, Shanghai 200125, China; Shanghai Institute of Precision Medicine, Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200125, ChinaLaboratory of Brain Atlas and Brain-inspired Intelligence, Institute of Automation, Chinese Academy of Sciences, Beijing 100190, China; School of Future Technology, University of Chinese Academy of Sciences, Beijing 101408, China; State Key Laboratory of Multimodal Artificial Intelligence Systems, Institute of Automation, Chinese Academy of Sciences, Beijing 100190, China; Corresponding authorDepartment of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People’s Hospital, Shanghai 200125, China; Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai 200125, China; Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases, Shanghai 200125, China; Shanghai Institute of Precision Medicine, Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200125, China; Corresponding authorSummary: In the mammalian cochlea, moderate acoustic overexposure leads to loss of ribbon-type synapse between the inner hair cell (IHC) and its postsynaptic spiral ganglion neuron (SGN), causing a reduced dynamic range of hearing but not a permanent threshold elevation. A prevailing view is that such ribbon loss (known as synaptopathy) selectively impacts the low-spontaneous-rate and high-threshold SGN fibers contacting predominantly the modiolar IHC face. However, the spatial pattern of synaptopathy remains scarcely characterized in the most sensitive mid-cochlear region, where two morphological subtypes of IHC with distinct ribbon size gradients coexist. Here, we used volume electron microscopy to investigate noise exposure-related changes in the mouse IHCs with and without ribbon loss. Our quantifications reveal that IHC subtypes differ in the worst-hit area of synaptopathy. Moreover, we show relative enrichment of mitochondria in the surviving SGN terminals, providing key experimental evidence for the long-proposed role of SGN-terminal mitochondria in synaptic vulnerability.http://www.sciencedirect.com/science/article/pii/S2589004224000464Biological sciencesNeuroscienceMolecular neuroscienceSensory neuroscience
spellingShingle Yan Lu
Jing Liu
Bei Li
Haoyu Wang
Fangfang Wang
Shengxiong Wang
Hao Wu
Hua Han
Yunfeng Hua
Spatial patterns of noise-induced inner hair cell ribbon loss in the mouse mid-cochlea
iScience
Biological sciences
Neuroscience
Molecular neuroscience
Sensory neuroscience
title Spatial patterns of noise-induced inner hair cell ribbon loss in the mouse mid-cochlea
title_full Spatial patterns of noise-induced inner hair cell ribbon loss in the mouse mid-cochlea
title_fullStr Spatial patterns of noise-induced inner hair cell ribbon loss in the mouse mid-cochlea
title_full_unstemmed Spatial patterns of noise-induced inner hair cell ribbon loss in the mouse mid-cochlea
title_short Spatial patterns of noise-induced inner hair cell ribbon loss in the mouse mid-cochlea
title_sort spatial patterns of noise induced inner hair cell ribbon loss in the mouse mid cochlea
topic Biological sciences
Neuroscience
Molecular neuroscience
Sensory neuroscience
url http://www.sciencedirect.com/science/article/pii/S2589004224000464
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