Network-level encoding of local neurotransmitters in cortical astrocytes

Autores
Cahill, Michelle K.; Collard, Max; Tse, Vincent; Reitman, Michael E.; Etchenique, Roberto Argentino; Kirst, Christoph; Poskanzer, Kira E.
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Astrocytes, the most abundant non-neuronal cell type in the mammalian brain, are crucial circuit components that respond to and modulate neuronal activity through calcium (Ca2+) signalling1–7 . Astrocyte Ca2+ activity is highly heterogeneous and occurs across multiple spatiotemporal scales—from fast, subcellular activity3,4 to slow, synchronized activity across connected astrocyte networks8–10—to infuence many processes5,7,11. However, the inputs that drive astrocyte network dynamics remain unclear. Here we used ex vivo and in vivo two-photon astrocyte imaging while mimicking neuronal neurotransmitter inputs at multiple spatiotemporal scales. We fnd that brief, subcellular inputs of GABA and glutamate lead to widespread, long-lasting astrocyte Ca2+ responses beyond an individual stimulated cell. Further, we fnd that a key subset of Ca2+ activity—propagative activity—diferentiates astrocyte network responses to these two main neurotransmitters, and may infuence responses to future inputs. Together, our results demonstrate that local, transient neurotransmitter inputs are encoded by broad cortical astrocyte networks over a minutes-long time course, contributing to accumulating evidence that substantial astrocyte–neuron communication occurs across slow, network-level spatiotemporal scales12–14. These fndings will enable future studies to investigate the link between specifc astrocyte Ca2+ activity and specifc functional outputs, which could build a consistent framework for astrocytic modulation of neuronal activity.
Fil: Cahill, Michelle K.. University of California; Estados Unidos
Fil: Collard, Max. University of California; Estados Unidos
Fil: Tse, Vincent. University of California; Estados Unidos
Fil: Reitman, Michael E.. University of California; Estados Unidos
Fil: Etchenique, Roberto Argentino. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química, Física de los Materiales, Medioambiente y Energía. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química, Física de los Materiales, Medioambiente y Energía; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Química Inorgánica, Analítica y Química Física; Argentina
Fil: Kirst, Christoph. University of California; Estados Unidos. Kavli Institute for Fundamental Neuroscience; Estados Unidos. Lawrence Berkeley National Laboratory; Estados Unidos
Fil: Poskanzer, Kira E.. University of California; Estados Unidos. Kavli Institute for Fundamental Neuroscience; Estados Unidos
Materia
Glia
Signaling
Caged neurotransmitters
Ruthenium
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:11336/262401

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spelling Network-level encoding of local neurotransmitters in cortical astrocytesCahill, Michelle K.Collard, MaxTse, VincentReitman, Michael E.Etchenique, Roberto ArgentinoKirst, ChristophPoskanzer, Kira E.GliaSignalingCaged neurotransmittersRutheniumhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Astrocytes, the most abundant non-neuronal cell type in the mammalian brain, are crucial circuit components that respond to and modulate neuronal activity through calcium (Ca2+) signalling1–7 . Astrocyte Ca2+ activity is highly heterogeneous and occurs across multiple spatiotemporal scales—from fast, subcellular activity3,4 to slow, synchronized activity across connected astrocyte networks8–10—to infuence many processes5,7,11. However, the inputs that drive astrocyte network dynamics remain unclear. Here we used ex vivo and in vivo two-photon astrocyte imaging while mimicking neuronal neurotransmitter inputs at multiple spatiotemporal scales. We fnd that brief, subcellular inputs of GABA and glutamate lead to widespread, long-lasting astrocyte Ca2+ responses beyond an individual stimulated cell. Further, we fnd that a key subset of Ca2+ activity—propagative activity—diferentiates astrocyte network responses to these two main neurotransmitters, and may infuence responses to future inputs. Together, our results demonstrate that local, transient neurotransmitter inputs are encoded by broad cortical astrocyte networks over a minutes-long time course, contributing to accumulating evidence that substantial astrocyte–neuron communication occurs across slow, network-level spatiotemporal scales12–14. These fndings will enable future studies to investigate the link between specifc astrocyte Ca2+ activity and specifc functional outputs, which could build a consistent framework for astrocytic modulation of neuronal activity.Fil: Cahill, Michelle K.. University of California; Estados UnidosFil: Collard, Max. University of California; Estados UnidosFil: Tse, Vincent. University of California; Estados UnidosFil: Reitman, Michael E.. University of California; Estados UnidosFil: Etchenique, Roberto Argentino. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química, Física de los Materiales, Medioambiente y Energía. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química, Física de los Materiales, Medioambiente y Energía; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Química Inorgánica, Analítica y Química Física; ArgentinaFil: Kirst, Christoph. University of California; Estados Unidos. Kavli Institute for Fundamental Neuroscience; Estados Unidos. Lawrence Berkeley National Laboratory; Estados UnidosFil: Poskanzer, Kira E.. University of California; Estados Unidos. Kavli Institute for Fundamental Neuroscience; Estados UnidosNature Publishing Group2024-04info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/262401Cahill, Michelle K.; Collard, Max; Tse, Vincent; Reitman, Michael E.; Etchenique, Roberto Argentino; et al.; Network-level encoding of local neurotransmitters in cortical astrocytes; Nature Publishing Group; Nature; 629; 8010; 4-2024; 146-1530028-0836CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41586-024-07311-5info:eu-repo/semantics/altIdentifier/doi/10.1038/s41586-024-07311-5info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:04:20Zoai:ri.conicet.gov.ar:11336/262401instacron: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:34982025-09-03 10:04:20.378CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Network-level encoding of local neurotransmitters in cortical astrocytes
title Network-level encoding of local neurotransmitters in cortical astrocytes
spellingShingle Network-level encoding of local neurotransmitters in cortical astrocytes
Cahill, Michelle K.
Glia
Signaling
Caged neurotransmitters
Ruthenium
title_short Network-level encoding of local neurotransmitters in cortical astrocytes
title_full Network-level encoding of local neurotransmitters in cortical astrocytes
title_fullStr Network-level encoding of local neurotransmitters in cortical astrocytes
title_full_unstemmed Network-level encoding of local neurotransmitters in cortical astrocytes
title_sort Network-level encoding of local neurotransmitters in cortical astrocytes
dc.creator.none.fl_str_mv Cahill, Michelle K.
Collard, Max
Tse, Vincent
Reitman, Michael E.
Etchenique, Roberto Argentino
Kirst, Christoph
Poskanzer, Kira E.
author Cahill, Michelle K.
author_facet Cahill, Michelle K.
Collard, Max
Tse, Vincent
Reitman, Michael E.
Etchenique, Roberto Argentino
Kirst, Christoph
Poskanzer, Kira E.
author_role author
author2 Collard, Max
Tse, Vincent
Reitman, Michael E.
Etchenique, Roberto Argentino
Kirst, Christoph
Poskanzer, Kira E.
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Glia
Signaling
Caged neurotransmitters
Ruthenium
topic Glia
Signaling
Caged neurotransmitters
Ruthenium
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Astrocytes, the most abundant non-neuronal cell type in the mammalian brain, are crucial circuit components that respond to and modulate neuronal activity through calcium (Ca2+) signalling1–7 . Astrocyte Ca2+ activity is highly heterogeneous and occurs across multiple spatiotemporal scales—from fast, subcellular activity3,4 to slow, synchronized activity across connected astrocyte networks8–10—to infuence many processes5,7,11. However, the inputs that drive astrocyte network dynamics remain unclear. Here we used ex vivo and in vivo two-photon astrocyte imaging while mimicking neuronal neurotransmitter inputs at multiple spatiotemporal scales. We fnd that brief, subcellular inputs of GABA and glutamate lead to widespread, long-lasting astrocyte Ca2+ responses beyond an individual stimulated cell. Further, we fnd that a key subset of Ca2+ activity—propagative activity—diferentiates astrocyte network responses to these two main neurotransmitters, and may infuence responses to future inputs. Together, our results demonstrate that local, transient neurotransmitter inputs are encoded by broad cortical astrocyte networks over a minutes-long time course, contributing to accumulating evidence that substantial astrocyte–neuron communication occurs across slow, network-level spatiotemporal scales12–14. These fndings will enable future studies to investigate the link between specifc astrocyte Ca2+ activity and specifc functional outputs, which could build a consistent framework for astrocytic modulation of neuronal activity.
Fil: Cahill, Michelle K.. University of California; Estados Unidos
Fil: Collard, Max. University of California; Estados Unidos
Fil: Tse, Vincent. University of California; Estados Unidos
Fil: Reitman, Michael E.. University of California; Estados Unidos
Fil: Etchenique, Roberto Argentino. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química, Física de los Materiales, Medioambiente y Energía. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química, Física de los Materiales, Medioambiente y Energía; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Química Inorgánica, Analítica y Química Física; Argentina
Fil: Kirst, Christoph. University of California; Estados Unidos. Kavli Institute for Fundamental Neuroscience; Estados Unidos. Lawrence Berkeley National Laboratory; Estados Unidos
Fil: Poskanzer, Kira E.. University of California; Estados Unidos. Kavli Institute for Fundamental Neuroscience; Estados Unidos
description Astrocytes, the most abundant non-neuronal cell type in the mammalian brain, are crucial circuit components that respond to and modulate neuronal activity through calcium (Ca2+) signalling1–7 . Astrocyte Ca2+ activity is highly heterogeneous and occurs across multiple spatiotemporal scales—from fast, subcellular activity3,4 to slow, synchronized activity across connected astrocyte networks8–10—to infuence many processes5,7,11. However, the inputs that drive astrocyte network dynamics remain unclear. Here we used ex vivo and in vivo two-photon astrocyte imaging while mimicking neuronal neurotransmitter inputs at multiple spatiotemporal scales. We fnd that brief, subcellular inputs of GABA and glutamate lead to widespread, long-lasting astrocyte Ca2+ responses beyond an individual stimulated cell. Further, we fnd that a key subset of Ca2+ activity—propagative activity—diferentiates astrocyte network responses to these two main neurotransmitters, and may infuence responses to future inputs. Together, our results demonstrate that local, transient neurotransmitter inputs are encoded by broad cortical astrocyte networks over a minutes-long time course, contributing to accumulating evidence that substantial astrocyte–neuron communication occurs across slow, network-level spatiotemporal scales12–14. These fndings will enable future studies to investigate the link between specifc astrocyte Ca2+ activity and specifc functional outputs, which could build a consistent framework for astrocytic modulation of neuronal activity.
publishDate 2024
dc.date.none.fl_str_mv 2024-04
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/11336/262401
Cahill, Michelle K.; Collard, Max; Tse, Vincent; Reitman, Michael E.; Etchenique, Roberto Argentino; et al.; Network-level encoding of local neurotransmitters in cortical astrocytes; Nature Publishing Group; Nature; 629; 8010; 4-2024; 146-153
0028-0836
CONICET Digital
CONICET
url http://hdl.handle.net/11336/262401
identifier_str_mv Cahill, Michelle K.; Collard, Max; Tse, Vincent; Reitman, Michael E.; Etchenique, Roberto Argentino; et al.; Network-level encoding of local neurotransmitters in cortical astrocytes; Nature Publishing Group; Nature; 629; 8010; 4-2024; 146-153
0028-0836
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41586-024-07311-5
info:eu-repo/semantics/altIdentifier/doi/10.1038/s41586-024-07311-5
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
dc.publisher.none.fl_str_mv Nature Publishing Group
publisher.none.fl_str_mv Nature Publishing Group
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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