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Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity

Mechanosensation – by which mechanical stimuli are converted into a neuronal signal – is the basis for the sensory systems of hearing, balance, and touch. Mechanosensation is unmatched in speed and its diverse range of sensitivities, reaching its highest temporal limits with the sense of hearing; ho...

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Autores principales: Perez-Flores, Maria C, Verschooten, Eric, Lee, Jeong Han, Kim, Hyo Jeong, Joris, Philip X, Yamoah, Ebenezer N
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8942473/
https://www.ncbi.nlm.nih.gov/pubmed/35266451
http://dx.doi.org/10.7554/eLife.74948
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author Perez-Flores, Maria C
Verschooten, Eric
Lee, Jeong Han
Kim, Hyo Jeong
Joris, Philip X
Yamoah, Ebenezer N
author_facet Perez-Flores, Maria C
Verschooten, Eric
Lee, Jeong Han
Kim, Hyo Jeong
Joris, Philip X
Yamoah, Ebenezer N
author_sort Perez-Flores, Maria C
collection PubMed
description Mechanosensation – by which mechanical stimuli are converted into a neuronal signal – is the basis for the sensory systems of hearing, balance, and touch. Mechanosensation is unmatched in speed and its diverse range of sensitivities, reaching its highest temporal limits with the sense of hearing; however, hair cells (HCs) and the auditory nerve (AN) serve as obligatory bottlenecks for sounds to engage the brain. Like other sensory neurons, auditory neurons use the canonical pathway for neurotransmission and millisecond-duration action potentials (APs). How the auditory system utilizes the relatively slow transmission mechanisms to achieve ultrafast speed, and high audio-frequency hearing remains an enigma. Here, we address this paradox and report that the mouse, and chinchilla, AN are mechanically sensitive, and minute mechanical displacement profoundly affects its response properties. Sound-mimicking sinusoidal mechanical and electrical current stimuli affect phase-locked responses. In a phase-dependent manner, the two stimuli can also evoke suppressive responses. We propose that mechanical sensitivity interacts with synaptic responses to shape responses in the AN, including frequency tuning and temporal phase locking. Combining neurotransmission and mechanical sensation to control spike patterns gives the mammalian AN a secondary receptor role, an emerging theme in primary neuronal functions.
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spelling pubmed-89424732022-03-24 Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity Perez-Flores, Maria C Verschooten, Eric Lee, Jeong Han Kim, Hyo Jeong Joris, Philip X Yamoah, Ebenezer N eLife Neuroscience Mechanosensation – by which mechanical stimuli are converted into a neuronal signal – is the basis for the sensory systems of hearing, balance, and touch. Mechanosensation is unmatched in speed and its diverse range of sensitivities, reaching its highest temporal limits with the sense of hearing; however, hair cells (HCs) and the auditory nerve (AN) serve as obligatory bottlenecks for sounds to engage the brain. Like other sensory neurons, auditory neurons use the canonical pathway for neurotransmission and millisecond-duration action potentials (APs). How the auditory system utilizes the relatively slow transmission mechanisms to achieve ultrafast speed, and high audio-frequency hearing remains an enigma. Here, we address this paradox and report that the mouse, and chinchilla, AN are mechanically sensitive, and minute mechanical displacement profoundly affects its response properties. Sound-mimicking sinusoidal mechanical and electrical current stimuli affect phase-locked responses. In a phase-dependent manner, the two stimuli can also evoke suppressive responses. We propose that mechanical sensitivity interacts with synaptic responses to shape responses in the AN, including frequency tuning and temporal phase locking. Combining neurotransmission and mechanical sensation to control spike patterns gives the mammalian AN a secondary receptor role, an emerging theme in primary neuronal functions. eLife Sciences Publications, Ltd 2022-03-10 /pmc/articles/PMC8942473/ /pubmed/35266451 http://dx.doi.org/10.7554/eLife.74948 Text en © 2022, Perez-Flores et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Perez-Flores, Maria C
Verschooten, Eric
Lee, Jeong Han
Kim, Hyo Jeong
Joris, Philip X
Yamoah, Ebenezer N
Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity
title Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity
title_full Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity
title_fullStr Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity
title_full_unstemmed Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity
title_short Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity
title_sort intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8942473/
https://www.ncbi.nlm.nih.gov/pubmed/35266451
http://dx.doi.org/10.7554/eLife.74948
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