Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity

Autores
Müller, Martin; Goutman, Juan Diego; Kochubey, Olexiy; Schneggenburger, Ralf
Año de publicación
2010
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The two fundamental forms of short-term plasticity, short-term depression and facilitation, coexist at most synapses, but little is known about their interaction. Here, we studied the interplay between short-term depression and facilitation at calyx of Held synapses. Stimulation at a "low" frequency of 10 or 20 Hz, which is in the range of the spontaneous activity of these auditory neurons in vivo, induced synaptic depression. Surprisingly, an instantaneous increase of the stimulation frequency to 100 or 200 Hz following the low-frequency train uncovered a robust facilitation of EPSCs relative to the predepressed amplitude level. This facilitation decayed rapidly (∼30 ms) and depended on presynaptic residual Ca2+, but it was not caused by Ca2+ current facilitation. To probe the release probability of the remaining readily releasable vesicles following the low-frequency train we made presynaptic Ca2+ uncaging experiments in the predepressed state of the synapse. We found that low-frequency stimulation depletes the fast-releasable vesicle pool (FRP) down to ∼40% of control and that the remaining FRP vesicles are released with ∼2-fold slower release kinetics, indicating a hitherto unknown intrinsic heterogeneity among FRP vesicles. Thus, vesicles with an intrinsically lower release probability predominate after low frequency stimulation and undergo facilitation during the onset of subsequent high-frequency trains. Facilitation in the predepressed state of the synapse might help to stabilize the amount of transmitter release at the onset of high-frequency firing at these auditory synapses.
Fil: Müller, Martin. Ecole Polytechnique Federale de Lausanne; Suiza
Fil: Goutman, Juan Diego. Ecole Polytechnique Federale de Lausanne; Suiza. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Kochubey, Olexiy. Ecole Polytechnique Federale de Lausanne; Suiza
Fil: Schneggenburger, Ralf. Ecole Polytechnique Federale de Lausanne; Suiza
Materia
synaptic transmission
facilitation
depression
exocytosis
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/53968

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network_name_str CONICET Digital (CONICET)
spelling Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticityMüller, MartinGoutman, Juan DiegoKochubey, OlexiySchneggenburger, Ralfsynaptic transmissionfacilitationdepressionexocytosishttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3The two fundamental forms of short-term plasticity, short-term depression and facilitation, coexist at most synapses, but little is known about their interaction. Here, we studied the interplay between short-term depression and facilitation at calyx of Held synapses. Stimulation at a "low" frequency of 10 or 20 Hz, which is in the range of the spontaneous activity of these auditory neurons in vivo, induced synaptic depression. Surprisingly, an instantaneous increase of the stimulation frequency to 100 or 200 Hz following the low-frequency train uncovered a robust facilitation of EPSCs relative to the predepressed amplitude level. This facilitation decayed rapidly (∼30 ms) and depended on presynaptic residual Ca2+, but it was not caused by Ca2+ current facilitation. To probe the release probability of the remaining readily releasable vesicles following the low-frequency train we made presynaptic Ca2+ uncaging experiments in the predepressed state of the synapse. We found that low-frequency stimulation depletes the fast-releasable vesicle pool (FRP) down to ∼40% of control and that the remaining FRP vesicles are released with ∼2-fold slower release kinetics, indicating a hitherto unknown intrinsic heterogeneity among FRP vesicles. Thus, vesicles with an intrinsically lower release probability predominate after low frequency stimulation and undergo facilitation during the onset of subsequent high-frequency trains. Facilitation in the predepressed state of the synapse might help to stabilize the amount of transmitter release at the onset of high-frequency firing at these auditory synapses.Fil: Müller, Martin. Ecole Polytechnique Federale de Lausanne; SuizaFil: Goutman, Juan Diego. Ecole Polytechnique Federale de Lausanne; Suiza. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Kochubey, Olexiy. Ecole Polytechnique Federale de Lausanne; SuizaFil: Schneggenburger, Ralf. Ecole Polytechnique Federale de Lausanne; SuizaSociety for Neuroscience2010-02info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/53968Müller, Martin; Goutman, Juan Diego; Kochubey, Olexiy; Schneggenburger, Ralf; Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity; Society for Neuroscience; Journal of Neuroscience; 30; 6; 2-2010; 2007-20160270-6474CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.4378-09.2010info:eu-repo/semantics/altIdentifier/url/http://www.jneurosci.org/content/30/6/2007info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:33:47Zoai:ri.conicet.gov.ar:11336/53968instacron: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 10:33:47.3CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity
title Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity
spellingShingle Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity
Müller, Martin
synaptic transmission
facilitation
depression
exocytosis
title_short Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity
title_full Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity
title_fullStr Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity
title_full_unstemmed Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity
title_sort Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity
dc.creator.none.fl_str_mv Müller, Martin
Goutman, Juan Diego
Kochubey, Olexiy
Schneggenburger, Ralf
author Müller, Martin
author_facet Müller, Martin
Goutman, Juan Diego
Kochubey, Olexiy
Schneggenburger, Ralf
author_role author
author2 Goutman, Juan Diego
Kochubey, Olexiy
Schneggenburger, Ralf
author2_role author
author
author
dc.subject.none.fl_str_mv synaptic transmission
facilitation
depression
exocytosis
topic synaptic transmission
facilitation
depression
exocytosis
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv The two fundamental forms of short-term plasticity, short-term depression and facilitation, coexist at most synapses, but little is known about their interaction. Here, we studied the interplay between short-term depression and facilitation at calyx of Held synapses. Stimulation at a "low" frequency of 10 or 20 Hz, which is in the range of the spontaneous activity of these auditory neurons in vivo, induced synaptic depression. Surprisingly, an instantaneous increase of the stimulation frequency to 100 or 200 Hz following the low-frequency train uncovered a robust facilitation of EPSCs relative to the predepressed amplitude level. This facilitation decayed rapidly (∼30 ms) and depended on presynaptic residual Ca2+, but it was not caused by Ca2+ current facilitation. To probe the release probability of the remaining readily releasable vesicles following the low-frequency train we made presynaptic Ca2+ uncaging experiments in the predepressed state of the synapse. We found that low-frequency stimulation depletes the fast-releasable vesicle pool (FRP) down to ∼40% of control and that the remaining FRP vesicles are released with ∼2-fold slower release kinetics, indicating a hitherto unknown intrinsic heterogeneity among FRP vesicles. Thus, vesicles with an intrinsically lower release probability predominate after low frequency stimulation and undergo facilitation during the onset of subsequent high-frequency trains. Facilitation in the predepressed state of the synapse might help to stabilize the amount of transmitter release at the onset of high-frequency firing at these auditory synapses.
Fil: Müller, Martin. Ecole Polytechnique Federale de Lausanne; Suiza
Fil: Goutman, Juan Diego. Ecole Polytechnique Federale de Lausanne; Suiza. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Kochubey, Olexiy. Ecole Polytechnique Federale de Lausanne; Suiza
Fil: Schneggenburger, Ralf. Ecole Polytechnique Federale de Lausanne; Suiza
description The two fundamental forms of short-term plasticity, short-term depression and facilitation, coexist at most synapses, but little is known about their interaction. Here, we studied the interplay between short-term depression and facilitation at calyx of Held synapses. Stimulation at a "low" frequency of 10 or 20 Hz, which is in the range of the spontaneous activity of these auditory neurons in vivo, induced synaptic depression. Surprisingly, an instantaneous increase of the stimulation frequency to 100 or 200 Hz following the low-frequency train uncovered a robust facilitation of EPSCs relative to the predepressed amplitude level. This facilitation decayed rapidly (∼30 ms) and depended on presynaptic residual Ca2+, but it was not caused by Ca2+ current facilitation. To probe the release probability of the remaining readily releasable vesicles following the low-frequency train we made presynaptic Ca2+ uncaging experiments in the predepressed state of the synapse. We found that low-frequency stimulation depletes the fast-releasable vesicle pool (FRP) down to ∼40% of control and that the remaining FRP vesicles are released with ∼2-fold slower release kinetics, indicating a hitherto unknown intrinsic heterogeneity among FRP vesicles. Thus, vesicles with an intrinsically lower release probability predominate after low frequency stimulation and undergo facilitation during the onset of subsequent high-frequency trains. Facilitation in the predepressed state of the synapse might help to stabilize the amount of transmitter release at the onset of high-frequency firing at these auditory synapses.
publishDate 2010
dc.date.none.fl_str_mv 2010-02
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/11336/53968
Müller, Martin; Goutman, Juan Diego; Kochubey, Olexiy; Schneggenburger, Ralf; Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity; Society for Neuroscience; Journal of Neuroscience; 30; 6; 2-2010; 2007-2016
0270-6474
CONICET Digital
CONICET
url http://hdl.handle.net/11336/53968
identifier_str_mv Müller, Martin; Goutman, Juan Diego; Kochubey, Olexiy; Schneggenburger, Ralf; Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity; Society for Neuroscience; Journal of Neuroscience; 30; 6; 2-2010; 2007-2016
0270-6474
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.4378-09.2010
info:eu-repo/semantics/altIdentifier/url/http://www.jneurosci.org/content/30/6/2007
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Society for Neuroscience
publisher.none.fl_str_mv Society for Neuroscience
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
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score 13.070432