Noise-induced ribbon synapse loss in the mouse basal cochlear region does not reduce inner hair cell exocytosis

Noise-induced hearing loss is one of the most common forms of hearing loss in adults and also one of the most common occupational diseases. Extensive previous work has shown that the highly sensitive synapses of the inner hair cells (IHCs) may be the first target for irreparable damage and permanent...

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Main Authors: David Oestreicher, Alfonso Mauro Malpede, Annalena Reitmeier, Carolin Paula Bräuer, Laura Schoch, Nicola Strenzke, Tina Pangrsic
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Cellular Neuroscience
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Online Access:https://www.frontiersin.org/articles/10.3389/fncel.2024.1523978/full
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author David Oestreicher
David Oestreicher
Alfonso Mauro Malpede
Alfonso Mauro Malpede
Annalena Reitmeier
Annalena Reitmeier
Carolin Paula Bräuer
Carolin Paula Bräuer
Laura Schoch
Laura Schoch
Nicola Strenzke
Nicola Strenzke
Tina Pangrsic
Tina Pangrsic
Tina Pangrsic
author_facet David Oestreicher
David Oestreicher
Alfonso Mauro Malpede
Alfonso Mauro Malpede
Annalena Reitmeier
Annalena Reitmeier
Carolin Paula Bräuer
Carolin Paula Bräuer
Laura Schoch
Laura Schoch
Nicola Strenzke
Nicola Strenzke
Tina Pangrsic
Tina Pangrsic
Tina Pangrsic
author_sort David Oestreicher
collection DOAJ
description Noise-induced hearing loss is one of the most common forms of hearing loss in adults and also one of the most common occupational diseases. Extensive previous work has shown that the highly sensitive synapses of the inner hair cells (IHCs) may be the first target for irreparable damage and permanent loss in the noise-exposed cochlea, more precisely in the cochlear base. However, how such synaptic loss affects the synaptic physiology of the IHCs in this particularly vulnerable part of the cochlea has not yet been investigated. To address this question, we exposed 3–4-week-old C57BL/6J mice to 8–16 kHz noise for 2 h under isoflurane anesthesia. We then employed hearing measurements, immunohistochemistry and patch-clamp to assess IHC synaptic function. Two noise sound pressure levels (SPLs) were used to evoke acute hearing threshold elevations with different levels of recovery 2 weeks post-exposure. Regardless of noise intensity, the exposure resulted in a loss of approximately 25–36% of ribbon synapses in the basal portions of the cochlea that persisted 2 weeks after exposure. Perforated patch-clamp recordings were made in the IHCs of the basal regions of the cochlea where the greatest synaptic losses were observed. Depolarization-evoked calcium currents in IHCs 2 weeks after exposure were slightly but not significantly smaller as compared to controls from age-matched non-exposed animals. Exocytic changes monitored as changes in membrane capacitance did not follow that trend and remained similar to controls despite significant loss of ribbons, likely reflecting increased exocytosis at the remaining synapses. Additionally, we report for the first time that acute application of isoflurane reduces IHC calcium currents, which may have implications for noise-induced IHC synaptic loss.
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spelling doaj-art-5daf41bfed464e099af2d9d506eb2cf82025-01-07T06:50:54ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022025-01-011810.3389/fncel.2024.15239781523978Noise-induced ribbon synapse loss in the mouse basal cochlear region does not reduce inner hair cell exocytosisDavid Oestreicher0David Oestreicher1Alfonso Mauro Malpede2Alfonso Mauro Malpede3Annalena Reitmeier4Annalena Reitmeier5Carolin Paula Bräuer6Carolin Paula Bräuer7Laura Schoch8Laura Schoch9Nicola Strenzke10Nicola Strenzke11Tina Pangrsic12Tina Pangrsic13Tina Pangrsic14Experimental Otology Group, InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, GermanyAuditory Neuroscience Group, Max Planck Institute for Multidisciplinary Sciences, Göttingen, GermanyExperimental Otology Group, InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, GermanyAuditory Neuroscience Group, Max Planck Institute for Multidisciplinary Sciences, Göttingen, GermanyExperimental Otology Group, InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, GermanyAuditory Neuroscience Group, Max Planck Institute for Multidisciplinary Sciences, Göttingen, GermanyExperimental Otology Group, InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, GermanyAuditory Neuroscience Group, Max Planck Institute for Multidisciplinary Sciences, Göttingen, GermanyExperimental Otology Group, InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, GermanyAuditory Neuroscience Group, Max Planck Institute for Multidisciplinary Sciences, Göttingen, GermanyAuditory Systems Physiology Group, Institute for Auditory Neuroscience, InnerEarLab, University Medical Center Göttingen, Göttingen, GermanyCollaborative Research Center 889, University of Göttingen, Göttingen, GermanyExperimental Otology Group, InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, GermanyAuditory Neuroscience Group, Max Planck Institute for Multidisciplinary Sciences, Göttingen, GermanyCollaborative Research Center 889, University of Göttingen, Göttingen, GermanyNoise-induced hearing loss is one of the most common forms of hearing loss in adults and also one of the most common occupational diseases. Extensive previous work has shown that the highly sensitive synapses of the inner hair cells (IHCs) may be the first target for irreparable damage and permanent loss in the noise-exposed cochlea, more precisely in the cochlear base. However, how such synaptic loss affects the synaptic physiology of the IHCs in this particularly vulnerable part of the cochlea has not yet been investigated. To address this question, we exposed 3–4-week-old C57BL/6J mice to 8–16 kHz noise for 2 h under isoflurane anesthesia. We then employed hearing measurements, immunohistochemistry and patch-clamp to assess IHC synaptic function. Two noise sound pressure levels (SPLs) were used to evoke acute hearing threshold elevations with different levels of recovery 2 weeks post-exposure. Regardless of noise intensity, the exposure resulted in a loss of approximately 25–36% of ribbon synapses in the basal portions of the cochlea that persisted 2 weeks after exposure. Perforated patch-clamp recordings were made in the IHCs of the basal regions of the cochlea where the greatest synaptic losses were observed. Depolarization-evoked calcium currents in IHCs 2 weeks after exposure were slightly but not significantly smaller as compared to controls from age-matched non-exposed animals. Exocytic changes monitored as changes in membrane capacitance did not follow that trend and remained similar to controls despite significant loss of ribbons, likely reflecting increased exocytosis at the remaining synapses. Additionally, we report for the first time that acute application of isoflurane reduces IHC calcium currents, which may have implications for noise-induced IHC synaptic loss.https://www.frontiersin.org/articles/10.3389/fncel.2024.1523978/fullinner hair cellnoise traumaribbon synapseisofluranecalcium channel
spellingShingle David Oestreicher
David Oestreicher
Alfonso Mauro Malpede
Alfonso Mauro Malpede
Annalena Reitmeier
Annalena Reitmeier
Carolin Paula Bräuer
Carolin Paula Bräuer
Laura Schoch
Laura Schoch
Nicola Strenzke
Nicola Strenzke
Tina Pangrsic
Tina Pangrsic
Tina Pangrsic
Noise-induced ribbon synapse loss in the mouse basal cochlear region does not reduce inner hair cell exocytosis
Frontiers in Cellular Neuroscience
inner hair cell
noise trauma
ribbon synapse
isoflurane
calcium channel
title Noise-induced ribbon synapse loss in the mouse basal cochlear region does not reduce inner hair cell exocytosis
title_full Noise-induced ribbon synapse loss in the mouse basal cochlear region does not reduce inner hair cell exocytosis
title_fullStr Noise-induced ribbon synapse loss in the mouse basal cochlear region does not reduce inner hair cell exocytosis
title_full_unstemmed Noise-induced ribbon synapse loss in the mouse basal cochlear region does not reduce inner hair cell exocytosis
title_short Noise-induced ribbon synapse loss in the mouse basal cochlear region does not reduce inner hair cell exocytosis
title_sort noise induced ribbon synapse loss in the mouse basal cochlear region does not reduce inner hair cell exocytosis
topic inner hair cell
noise trauma
ribbon synapse
isoflurane
calcium channel
url https://www.frontiersin.org/articles/10.3389/fncel.2024.1523978/full
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