Sound exposure dynamically induces dopamine synthesis in cholinergic LOC efferents for feedback to auditory nerve fibers

Lateral olivocochlear (LOC) efferent neurons modulate auditory nerve fiber (ANF) activity using a large repertoire of neurotransmitters, including dopamine (DA) and acetylcholine (ACh). Little is known about how individual neurotransmitter systems are differentially utilized in response to the ever-...

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Main Authors: Jingjing Sherry Wu, Eunyoung Yi, Marco Manca, Hamad Javaid, Amanda M Lauer, Elisabeth Glowatzki
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/52419
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spelling doaj-d3ef715b83414d75ae0d886e5f6ea2c12021-05-05T20:46:18ZengeLife Sciences Publications LtdeLife2050-084X2020-01-01910.7554/eLife.52419Sound exposure dynamically induces dopamine synthesis in cholinergic LOC efferents for feedback to auditory nerve fibersJingjing Sherry Wu0https://orcid.org/0000-0001-9625-1661Eunyoung Yi1Marco Manca2Hamad Javaid3Amanda M Lauer4https://orcid.org/0000-0003-4184-7374Elisabeth Glowatzki5https://orcid.org/0000-0003-3135-658XDepartment of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States; The Center for Sensory Biology, The Johns Hopkins University School of Medicine, Baltimore, United States; The Center for Hearing and Balance, The Johns Hopkins University School of Medicine, Baltimore, United StatesCollege of Pharmacy and Natural Medicine Research Institute, Mokpo National University, Muan-gun, Republic of KoreaThe Center for Sensory Biology, The Johns Hopkins University School of Medicine, Baltimore, United States; The Center for Hearing and Balance, The Johns Hopkins University School of Medicine, Baltimore, United States; Department of Otolaryngology-Head and Neck Surgery, The Johns Hopkins University School of Medicine, Baltimore, United StatesThe Center for Sensory Biology, The Johns Hopkins University School of Medicine, Baltimore, United States; The Center for Hearing and Balance, The Johns Hopkins University School of Medicine, Baltimore, United States; Department of Otolaryngology-Head and Neck Surgery, The Johns Hopkins University School of Medicine, Baltimore, United StatesThe Center for Sensory Biology, The Johns Hopkins University School of Medicine, Baltimore, United States; The Center for Hearing and Balance, The Johns Hopkins University School of Medicine, Baltimore, United States; Department of Otolaryngology-Head and Neck Surgery, The Johns Hopkins University School of Medicine, Baltimore, United StatesDepartment of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States; The Center for Sensory Biology, The Johns Hopkins University School of Medicine, Baltimore, United States; The Center for Hearing and Balance, The Johns Hopkins University School of Medicine, Baltimore, United States; Department of Otolaryngology-Head and Neck Surgery, The Johns Hopkins University School of Medicine, Baltimore, United StatesLateral olivocochlear (LOC) efferent neurons modulate auditory nerve fiber (ANF) activity using a large repertoire of neurotransmitters, including dopamine (DA) and acetylcholine (ACh). Little is known about how individual neurotransmitter systems are differentially utilized in response to the ever-changing acoustic environment. Here we present quantitative evidence in rodents that the dopaminergic LOC input to ANFs is dynamically regulated according to the animal’s recent acoustic experience. Sound exposure upregulates tyrosine hydroxylase, an enzyme responsible for dopamine synthesis, in cholinergic LOC intrinsic neurons, suggesting that individual LOC neurons might at times co-release ACh and DA. We further demonstrate that dopamine down-regulates ANF firing rates by reducing both the hair cell release rate and the size of synaptic events. Collectively, our results suggest that LOC intrinsic neurons can undergo on-demand neurotransmitter re-specification to re-calibrate ANF activity, adjust the gain at hair cell/ANF synapses, and possibly to protect these synapses from noise damage.https://elifesciences.org/articles/52419auditory nerve fiberspiral ganglion neuronolivocochlear efferentsdopamineacetylcholinenoise damage
collection DOAJ
language English
format Article
sources DOAJ
author Jingjing Sherry Wu
Eunyoung Yi
Marco Manca
Hamad Javaid
Amanda M Lauer
Elisabeth Glowatzki
spellingShingle Jingjing Sherry Wu
Eunyoung Yi
Marco Manca
Hamad Javaid
Amanda M Lauer
Elisabeth Glowatzki
Sound exposure dynamically induces dopamine synthesis in cholinergic LOC efferents for feedback to auditory nerve fibers
eLife
auditory nerve fiber
spiral ganglion neuron
olivocochlear efferents
dopamine
acetylcholine
noise damage
author_facet Jingjing Sherry Wu
Eunyoung Yi
Marco Manca
Hamad Javaid
Amanda M Lauer
Elisabeth Glowatzki
author_sort Jingjing Sherry Wu
title Sound exposure dynamically induces dopamine synthesis in cholinergic LOC efferents for feedback to auditory nerve fibers
title_short Sound exposure dynamically induces dopamine synthesis in cholinergic LOC efferents for feedback to auditory nerve fibers
title_full Sound exposure dynamically induces dopamine synthesis in cholinergic LOC efferents for feedback to auditory nerve fibers
title_fullStr Sound exposure dynamically induces dopamine synthesis in cholinergic LOC efferents for feedback to auditory nerve fibers
title_full_unstemmed Sound exposure dynamically induces dopamine synthesis in cholinergic LOC efferents for feedback to auditory nerve fibers
title_sort sound exposure dynamically induces dopamine synthesis in cholinergic loc efferents for feedback to auditory nerve fibers
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-01-01
description Lateral olivocochlear (LOC) efferent neurons modulate auditory nerve fiber (ANF) activity using a large repertoire of neurotransmitters, including dopamine (DA) and acetylcholine (ACh). Little is known about how individual neurotransmitter systems are differentially utilized in response to the ever-changing acoustic environment. Here we present quantitative evidence in rodents that the dopaminergic LOC input to ANFs is dynamically regulated according to the animal’s recent acoustic experience. Sound exposure upregulates tyrosine hydroxylase, an enzyme responsible for dopamine synthesis, in cholinergic LOC intrinsic neurons, suggesting that individual LOC neurons might at times co-release ACh and DA. We further demonstrate that dopamine down-regulates ANF firing rates by reducing both the hair cell release rate and the size of synaptic events. Collectively, our results suggest that LOC intrinsic neurons can undergo on-demand neurotransmitter re-specification to re-calibrate ANF activity, adjust the gain at hair cell/ANF synapses, and possibly to protect these synapses from noise damage.
topic auditory nerve fiber
spiral ganglion neuron
olivocochlear efferents
dopamine
acetylcholine
noise damage
url https://elifesciences.org/articles/52419
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