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

Autores
Johnson, Stuart L.; Wedemeyer, Carolina; Vetter, Douglas E.; Adachi, Roberto; Holley, Matthew C.; Elgoyhen, Ana Belen; Marcotti, Walter
Año de publicación
2013
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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 Ca2+-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.
Fil: Johnson, Stuart L.. University of Sheffield. Department of Biomedical Science; Reino Unido
Fil: Wedemeyer, Carolina. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular; Argentina
Fil: Vetter, Douglas E.. University of Mississippi Medical Center. Department of Neurobiology and Anatomical Sciences; Estados Unidos
Fil: Adachi, Roberto. The University of Texas. MD Anderson Cancer Center. Department of Pulmonary Medicine; Estados Unidos
Fil: Holley, Matthew C.. University of Sheffield. Department of Biomedical Science; Reino Unido
Fil: Elgoyhen, Ana Belen. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular; Argentina
Fil: Marcotti, Walter. University of Sheffield. Department of Biomedical Science; Reino Unido
Materia
Hair cells
Critical period
Development
Cochlea
Calcium current
Exocytosis
Efferent system
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/4013
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/4013
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapsesJohnson, Stuart L.Wedemeyer, CarolinaVetter, Douglas E.Adachi, RobertoHolley, Matthew C.Elgoyhen, Ana BelenMarcotti, WalterHair cellsCritical periodDevelopmentCochleaCalcium currentExocytosisEfferent systemhttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3Spontaneous 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 Ca2+-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.Fil: Johnson, Stuart L.. University of Sheffield. Department of Biomedical Science; Reino UnidoFil: Wedemeyer, Carolina. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular; ArgentinaFil: Vetter, Douglas E.. University of Mississippi Medical Center. Department of Neurobiology and Anatomical Sciences; Estados UnidosFil: Adachi, Roberto. The University of Texas. MD Anderson Cancer Center. Department of Pulmonary Medicine; Estados UnidosFil: Holley, Matthew C.. University of Sheffield. Department of Biomedical Science; Reino UnidoFil: Elgoyhen, Ana Belen. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular; ArgentinaFil: Marcotti, Walter. University of Sheffield. Department of Biomedical Science; Reino UnidoThe Royal Society2013-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/4013Johnson, Stuart L.; Wedemeyer, Carolina; Vetter, Douglas E.; Adachi, Roberto; Holley, Matthew C.; et al.; Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses; The Royal Society; Open Biology; 3; 11; 6-2013; 130163-1301632046-2441enginfo:eu-repo/semantics/altIdentifier/url/http://rsob.royalsocietypublishing.org/content/3/11/130163.longinfo:eu-repo/semantics/altIdentifier/doi/10.1098%2Frsob.130163info:eu-repo/semantics/altIdentifier/url/http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3843824/info:eu-repo/semantics/altIdentifier/issn/2046-2441info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:48:41Zoai:ri.conicet.gov.ar:11336/4013instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:48:42.22CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv 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
spellingShingle Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses
Johnson, Stuart L.
Hair cells
Critical period
Development
Cochlea
Calcium current
Exocytosis
Efferent system
title_short 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_sort Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses
dc.creator.none.fl_str_mv Johnson, Stuart L.
Wedemeyer, Carolina
Vetter, Douglas E.
Adachi, Roberto
Holley, Matthew C.
Elgoyhen, Ana Belen
Marcotti, Walter
author Johnson, Stuart L.
author_facet Johnson, Stuart L.
Wedemeyer, Carolina
Vetter, Douglas E.
Adachi, Roberto
Holley, Matthew C.
Elgoyhen, Ana Belen
Marcotti, Walter
author_role author
author2 Wedemeyer, Carolina
Vetter, Douglas E.
Adachi, Roberto
Holley, Matthew C.
Elgoyhen, Ana Belen
Marcotti, Walter
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Hair cells
Critical period
Development
Cochlea
Calcium current
Exocytosis
Efferent system
topic Hair cells
Critical period
Development
Cochlea
Calcium current
Exocytosis
Efferent system
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv 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 Ca2+-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.
Fil: Johnson, Stuart L.. University of Sheffield. Department of Biomedical Science; Reino Unido
Fil: Wedemeyer, Carolina. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular; Argentina
Fil: Vetter, Douglas E.. University of Mississippi Medical Center. Department of Neurobiology and Anatomical Sciences; Estados Unidos
Fil: Adachi, Roberto. The University of Texas. MD Anderson Cancer Center. Department of Pulmonary Medicine; Estados Unidos
Fil: Holley, Matthew C.. University of Sheffield. Department of Biomedical Science; Reino Unido
Fil: Elgoyhen, Ana Belen. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular; Argentina
Fil: Marcotti, Walter. University of Sheffield. Department of Biomedical Science; Reino Unido
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 Ca2+-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.
publishDate 2013
dc.date.none.fl_str_mv 2013-06
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/4013
Johnson, Stuart L.; Wedemeyer, Carolina; Vetter, Douglas E.; Adachi, Roberto; Holley, Matthew C.; et al.; Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses; The Royal Society; Open Biology; 3; 11; 6-2013; 130163-130163
2046-2441
url http://hdl.handle.net/11336/4013
identifier_str_mv Johnson, Stuart L.; Wedemeyer, Carolina; Vetter, Douglas E.; Adachi, Roberto; Holley, Matthew C.; et al.; Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses; The Royal Society; Open Biology; 3; 11; 6-2013; 130163-130163
2046-2441
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://rsob.royalsocietypublishing.org/content/3/11/130163.long
info:eu-repo/semantics/altIdentifier/doi/10.1098%2Frsob.130163
info:eu-repo/semantics/altIdentifier/url/http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3843824/
info:eu-repo/semantics/altIdentifier/issn/2046-2441
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv The Royal Society
publisher.none.fl_str_mv The Royal Society
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
_version_ 1844613511449149440
score 13.070432

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