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Research Articles, Cellular/Molecular

In Vivo Optogenetics Reveals Control of Cochlear Electromechanical Responses by Supporting Cells

Victoria A. Lukashkina, Snezana Levic, Patrício Simões, Zhenhang Xu, Joseph A. DiGuiseppi, Jian Zuo, Andrei N. Lukashin and Ian J. Russell
Journal of Neuroscience 20 July 2022, 42 (29) 5660-5671; DOI: https://doi.org/10.1523/JNEUROSCI.2127-21.2022
Victoria A. Lukashkina
1Sensory Neuroscience Research Group, School of Applied Sciences, University of Brighton, Brighton, BN2 4GJ, United Kingdom
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Snezana Levic
1Sensory Neuroscience Research Group, School of Applied Sciences, University of Brighton, Brighton, BN2 4GJ, United Kingdom
3Brighton and Sussex Medical School, University of Sussex, Brighton, BN1 9PX, United Kingdom
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Patrício Simões
1Sensory Neuroscience Research Group, School of Applied Sciences, University of Brighton, Brighton, BN2 4GJ, United Kingdom
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Zhenhang Xu
2Department of Biomedical Sciences, Creighton University School of Medicine, Omaha, Nebraska 68178
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Joseph A. DiGuiseppi
2Department of Biomedical Sciences, Creighton University School of Medicine, Omaha, Nebraska 68178
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Jian Zuo
2Department of Biomedical Sciences, Creighton University School of Medicine, Omaha, Nebraska 68178
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Andrei N. Lukashin
1Sensory Neuroscience Research Group, School of Applied Sciences, University of Brighton, Brighton, BN2 4GJ, United Kingdom
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Ian J. Russell
1Sensory Neuroscience Research Group, School of Applied Sciences, University of Brighton, Brighton, BN2 4GJ, United Kingdom
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Abstract

Cochlear sensitivity, essential for communication and exploiting the acoustic environment, results from sensory-motor outer hair cells (OHCs) operating in a structural scaffold of supporting cells and extracellular cortilymph within the organ of Corti (OoC). Cochlear sensitivity control is hypothesized to involve interaction between the OHCs and OoC supporting cells (e.g., Deiters' cells [DCs] and outer pillar cells [OPCs]), but this has never been established in vivo. Here, we conditionally expressed channelrhodopsins (ChR2) specifically in male and female mouse DCs and OPCs. Illumination of the OoC activated the nonselective ChR2 cation conductance and depolarized DCs when measured in vivo and in isolated OoC. Measurements of sound-induced cochlear mechanical and electrical responses revealed that OoC illumination suppressed the normal functions of OoC supporting cells transiently and reversibly. OoC illumination blocked normally occurring continuous minor adjustments of tone-evoked basilar membrane displacements over their entire dynamic range and OHC voltage responses to tones at levels and frequencies subject to cochlear amplification. OoC illumination altered the OHC mechanoelectrical transduction conductance operating point, which reversed the asymmetry of OHC voltage responses to high level tones. OoC illumination accelerated recovery from temporary loud sound-induced acoustic desensitization. We concluded that DCs and OPCs are involved in both the control of cochlear responses (which are essential for normal hearing) and the recovery from temporary acoustic desensitization. This is the first direct in vivo evidence for the interdependency of the structural, mechanical, and electrochemical arrangements of OHCs and OoC supporting cells that together provide fine control of cochlear responses.

SIGNIFICANCE STATEMENT A striking feature of the mammalian cochlear sensory epithelium, the organ of Corti, is the cellular architecture and supporting cell arrangement that provides a structural scaffold for the sensory-motor outer hair cells. The role of the supporting cell scaffold, however, has never been elucidated in vivo, although in vitro and modeling studies indicate the scaffold is involved in exchange of forces between the outer hair cells and the organ of Corti. We used in vivo techniques, including optogenetics, that do not disrupt arrangements between the outer hair cells and supporting cells, but selectively, transiently, and reversibly interfere with supporting cell normal function. We revealed the supporting cells provide continuous adjustment of cochlear sensitivity, which is instrumental in normal hearing.

  • cochlea
  • cochlear amplifier
  • cochlear supporting cells
  • optogenetics
  • organ of Corti
  • outer hair cells

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The Journal of Neuroscience: 42 (29)
Journal of Neuroscience
Vol. 42, Issue 29
20 Jul 2022
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In Vivo Optogenetics Reveals Control of Cochlear Electromechanical Responses by Supporting Cells
Victoria A. Lukashkina, Snezana Levic, Patrício Simões, Zhenhang Xu, Joseph A. DiGuiseppi, Jian Zuo, Andrei N. Lukashin, Ian J. Russell
Journal of Neuroscience 20 July 2022, 42 (29) 5660-5671; DOI: 10.1523/JNEUROSCI.2127-21.2022

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In Vivo Optogenetics Reveals Control of Cochlear Electromechanical Responses by Supporting Cells
Victoria A. Lukashkina, Snezana Levic, Patrício Simões, Zhenhang Xu, Joseph A. DiGuiseppi, Jian Zuo, Andrei N. Lukashin, Ian J. Russell
Journal of Neuroscience 20 July 2022, 42 (29) 5660-5671; DOI: 10.1523/JNEUROSCI.2127-21.2022
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Keywords

  • cochlea
  • cochlear amplifier
  • cochlear supporting cells
  • optogenetics
  • organ of Corti
  • outer hair cells

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