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Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses

Spontaneous electrical activity generated by developing sensory cells and neurons is crucial for the maturation of neural circuits. The full maturation of mammalian auditory inner hair cells (IHCs) depends on patterns of spontaneous action potentials during a ‘critical period’ of development. The in...

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Autores principales: Johnson, Stuart L., Wedemeyer, Carolina, Vetter, Douglas E., Adachi, Roberto, Holley, Matthew C., Elgoyhen, Ana Belén, Marcotti, Walter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3843824/
https://www.ncbi.nlm.nih.gov/pubmed/24350389
http://dx.doi.org/10.1098/rsob.130163
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author Johnson, Stuart L.
Wedemeyer, Carolina
Vetter, Douglas E.
Adachi, Roberto
Holley, Matthew C.
Elgoyhen, Ana Belén
Marcotti, Walter
author_facet Johnson, Stuart L.
Wedemeyer, Carolina
Vetter, Douglas E.
Adachi, Roberto
Holley, Matthew C.
Elgoyhen, Ana Belén
Marcotti, Walter
author_sort Johnson, Stuart L.
collection PubMed
description Spontaneous electrical activity generated by developing sensory cells and neurons is crucial for the maturation of neural circuits. The full maturation of mammalian auditory inner hair cells (IHCs) depends on patterns of spontaneous action potentials during a ‘critical period’ of development. The intrinsic spiking activity of IHCs can be modulated by inhibitory input from cholinergic efferent fibres descending from the brainstem, which transiently innervate immature IHCs. However, it remains unknown whether this transient efferent input to developing IHCs is required for their functional maturation. We used a mouse model that lacks the α9-nicotinic acetylcholine receptor subunit (α9nAChR) in IHCs and another lacking synaptotagmin-2 in the efferent terminals to remove or reduce efferent input to IHCs, respectively. We found that the efferent system is required for the developmental linearization of the Ca(2+)-sensitivity of vesicle fusion at IHC ribbon synapses, without affecting their general cell development. This provides the first direct evidence that the efferent system, by modulating IHC electrical activity, is required for the maturation of the IHC synaptic machinery. The central control of sensory cell development is unique among sensory systems.
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spelling pubmed-38438242013-12-13 Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses Johnson, Stuart L. Wedemeyer, Carolina Vetter, Douglas E. Adachi, Roberto Holley, Matthew C. Elgoyhen, Ana Belén Marcotti, Walter Open Biol Research Spontaneous electrical activity generated by developing sensory cells and neurons is crucial for the maturation of neural circuits. The full maturation of mammalian auditory inner hair cells (IHCs) depends on patterns of spontaneous action potentials during a ‘critical period’ of development. The intrinsic spiking activity of IHCs can be modulated by inhibitory input from cholinergic efferent fibres descending from the brainstem, which transiently innervate immature IHCs. However, it remains unknown whether this transient efferent input to developing IHCs is required for their functional maturation. We used a mouse model that lacks the α9-nicotinic acetylcholine receptor subunit (α9nAChR) in IHCs and another lacking synaptotagmin-2 in the efferent terminals to remove or reduce efferent input to IHCs, respectively. We found that the efferent system is required for the developmental linearization of the Ca(2+)-sensitivity of vesicle fusion at IHC ribbon synapses, without affecting their general cell development. This provides the first direct evidence that the efferent system, by modulating IHC electrical activity, is required for the maturation of the IHC synaptic machinery. The central control of sensory cell development is unique among sensory systems. The Royal Society 2013-11 /pmc/articles/PMC3843824/ /pubmed/24350389 http://dx.doi.org/10.1098/rsob.130163 Text en http://creativecommons.org/licenses/by/3.0/ © 2013 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Research
Johnson, Stuart L.
Wedemeyer, Carolina
Vetter, Douglas E.
Adachi, Roberto
Holley, Matthew C.
Elgoyhen, Ana Belén
Marcotti, Walter
Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses
title Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses
title_full Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses
title_fullStr Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses
title_full_unstemmed Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses
title_short Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses
title_sort cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3843824/
https://www.ncbi.nlm.nih.gov/pubmed/24350389
http://dx.doi.org/10.1098/rsob.130163
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