Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus

Autores
Krzisch, Marine; Temprana, Silvio Gabriel; Mongiat, Lucas Alberto; Armida, Jan; Schmutz, Valentin; Virtanen, Mari A.; Kocher Braissant, Jacqueline; Kraftsik, Rudolf; Vutskits, Laszlo; Conzelmann, Karl Klaus; Bergami, Matteo; Gage, Fred H.; Schinder, Alejandro Fabian; Toni, Nicolas
Año de publicación
2015
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The adult dentate gyrus produces new neurons that morphologically and functionally integrate into the hippocampal network. In the adult brain, most excitatory synapses are ensheathed by astrocytic perisynaptic processes that regulate synaptic structure and function. However, these processes are formed during embryonic or early postnatal development and it is unknown whether astrocytes can also ensheathe synapses of neurons born during adulthood and, if so, whether they play a role in their synaptic transmission. Here, we used a combination of serial-section immuno-electron microscopy, confocal microscopy, and electrophysiology to examine the formation of perisynaptic processes on adult-born neurons. We found that the afferent and efferent synapses of newborn neurons are ensheathed by astrocytic processes, irrespective of the age of the neurons or the size of their synapses. The quantification of gliogenesis and the distribution of astrocytic processes on synapses formed by adult-born neurons suggest that the majority of these processes are recruited from pre-existing astrocytes. Furthermore, the inhibition of astrocytic glutamate re-uptake significantly reduced postsynaptic currents and increased paired-pulse facilitation in adult-born neurons, suggesting that perisynaptic processes modulate synaptic transmission on these cells. Finally, some processes were found intercalated between newly formed dendritic spines and potential presynaptic partners, suggesting that they may also play a structural role in the connectivity of new spines. Together, these results indicate that pre-existing astrocytes remodel their processes to ensheathe synapses of adult-born neurons and participate to the functional and structural integration of these cells into the hippocampal network.
Fil: Krzisch, Marine. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Fil: Temprana, Silvio Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquimicas de Buenos Aires; Argentina. Fundación Instituto Leloir; Argentina
Fil: Mongiat, Lucas Alberto. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquimicas de Buenos Aires; Argentina. Fundación Instituto Leloir; Argentina
Fil: Armida, Jan. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Fil: Schmutz, Valentin. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Fil: Virtanen, Mari A.. Universidad de Ginebra; Suiza
Fil: Kocher Braissant, Jacqueline. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Fil: Kraftsik, Rudolf. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Fil: Vutskits, Laszlo. Universidad de Ginebra; Suiza. University Hospital of Geneva. Department of Anesthesiology, Pharmacology and Intensive Care; Suiza
Fil: Conzelmann, Karl Klaus. Ludwig-Maximilians University Múnich. Max von Pettenkofer Institute and Gene Center; Alemania
Fil: Bergami, Matteo. University Hospital of Cologne; Alemania
Fil: Gage, Fred H.. Salk Institute for Biological Studies; Estados Unidos
Fil: Schinder, Alejandro Fabian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquimicas de Buenos Aires; Argentina. Fundación Instituto Leloir; Argentina
Fil: Toni, Nicolas. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Materia
Adult neurogenesis
Dentate gyrus
Synaptogenesis
Astrocytes
Perisynaptic processes
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:11336/9313
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/9313
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampusKrzisch, MarineTemprana, Silvio GabrielMongiat, Lucas AlbertoArmida, JanSchmutz, ValentinVirtanen, Mari A.Kocher Braissant, JacquelineKraftsik, RudolfVutskits, LaszloConzelmann, Karl KlausBergami, MatteoGage, Fred H.Schinder, Alejandro FabianToni, NicolasAdult neurogenesisDentate gyrusSynaptogenesisAstrocytesPerisynaptic processeshttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3The adult dentate gyrus produces new neurons that morphologically and functionally integrate into the hippocampal network. In the adult brain, most excitatory synapses are ensheathed by astrocytic perisynaptic processes that regulate synaptic structure and function. However, these processes are formed during embryonic or early postnatal development and it is unknown whether astrocytes can also ensheathe synapses of neurons born during adulthood and, if so, whether they play a role in their synaptic transmission. Here, we used a combination of serial-section immuno-electron microscopy, confocal microscopy, and electrophysiology to examine the formation of perisynaptic processes on adult-born neurons. We found that the afferent and efferent synapses of newborn neurons are ensheathed by astrocytic processes, irrespective of the age of the neurons or the size of their synapses. The quantification of gliogenesis and the distribution of astrocytic processes on synapses formed by adult-born neurons suggest that the majority of these processes are recruited from pre-existing astrocytes. Furthermore, the inhibition of astrocytic glutamate re-uptake significantly reduced postsynaptic currents and increased paired-pulse facilitation in adult-born neurons, suggesting that perisynaptic processes modulate synaptic transmission on these cells. Finally, some processes were found intercalated between newly formed dendritic spines and potential presynaptic partners, suggesting that they may also play a structural role in the connectivity of new spines. Together, these results indicate that pre-existing astrocytes remodel their processes to ensheathe synapses of adult-born neurons and participate to the functional and structural integration of these cells into the hippocampal network.Fil: Krzisch, Marine. University of Lausanne. Department of Fundamental Neurosciences; SuizaFil: Temprana, Silvio Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquimicas de Buenos Aires; Argentina. Fundación Instituto Leloir; ArgentinaFil: Mongiat, Lucas Alberto. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquimicas de Buenos Aires; Argentina. Fundación Instituto Leloir; ArgentinaFil: Armida, Jan. University of Lausanne. Department of Fundamental Neurosciences; SuizaFil: Schmutz, Valentin. University of Lausanne. Department of Fundamental Neurosciences; SuizaFil: Virtanen, Mari A.. Universidad de Ginebra; SuizaFil: Kocher Braissant, Jacqueline. University of Lausanne. Department of Fundamental Neurosciences; SuizaFil: Kraftsik, Rudolf. University of Lausanne. Department of Fundamental Neurosciences; SuizaFil: Vutskits, Laszlo. Universidad de Ginebra; Suiza. University Hospital of Geneva. Department of Anesthesiology, Pharmacology and Intensive Care; SuizaFil: Conzelmann, Karl Klaus. Ludwig-Maximilians University Múnich. Max von Pettenkofer Institute and Gene Center; AlemaniaFil: Bergami, Matteo. University Hospital of Cologne; AlemaniaFil: Gage, Fred H.. Salk Institute for Biological Studies; Estados UnidosFil: Schinder, Alejandro Fabian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquimicas de Buenos Aires; Argentina. Fundación Instituto Leloir; ArgentinaFil: Toni, Nicolas. University of Lausanne. Department of Fundamental Neurosciences; SuizaSpringer Heidelberg2015-07info: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/11336/9313Krzisch, Marine; Temprana, Silvio Gabriel; Mongiat, Lucas Alberto; Armida, Jan; Schmutz, Valentin; et al.; Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus; Springer Heidelberg; Brain Structure & Function; 220; 4; 7-2015; 2027-20421863-2653enginfo:eu-repo/semantics/altIdentifier/url/http://link.springer.com/article/10.1007%2Fs00429-014-0768-yinfo:eu-repo/semantics/altIdentifier/doi/10.1007/s00429-014-0768-yinfo:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4481333/info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:52:22Zoai:ri.conicet.gov.ar:11336/9313instacron: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 09:52:22.929CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus
title Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus
spellingShingle Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus
Krzisch, Marine
Adult neurogenesis
Dentate gyrus
Synaptogenesis
Astrocytes
Perisynaptic processes
title_short Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus
title_full Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus
title_fullStr Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus
title_full_unstemmed Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus
title_sort Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus
dc.creator.none.fl_str_mv Krzisch, Marine
Temprana, Silvio Gabriel
Mongiat, Lucas Alberto
Armida, Jan
Schmutz, Valentin
Virtanen, Mari A.
Kocher Braissant, Jacqueline
Kraftsik, Rudolf
Vutskits, Laszlo
Conzelmann, Karl Klaus
Bergami, Matteo
Gage, Fred H.
Schinder, Alejandro Fabian
Toni, Nicolas
author Krzisch, Marine
author_facet Krzisch, Marine
Temprana, Silvio Gabriel
Mongiat, Lucas Alberto
Armida, Jan
Schmutz, Valentin
Virtanen, Mari A.
Kocher Braissant, Jacqueline
Kraftsik, Rudolf
Vutskits, Laszlo
Conzelmann, Karl Klaus
Bergami, Matteo
Gage, Fred H.
Schinder, Alejandro Fabian
Toni, Nicolas
author_role author
author2 Temprana, Silvio Gabriel
Mongiat, Lucas Alberto
Armida, Jan
Schmutz, Valentin
Virtanen, Mari A.
Kocher Braissant, Jacqueline
Kraftsik, Rudolf
Vutskits, Laszlo
Conzelmann, Karl Klaus
Bergami, Matteo
Gage, Fred H.
Schinder, Alejandro Fabian
Toni, Nicolas
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Adult neurogenesis
Dentate gyrus
Synaptogenesis
Astrocytes
Perisynaptic processes
topic Adult neurogenesis
Dentate gyrus
Synaptogenesis
Astrocytes
Perisynaptic processes
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 adult dentate gyrus produces new neurons that morphologically and functionally integrate into the hippocampal network. In the adult brain, most excitatory synapses are ensheathed by astrocytic perisynaptic processes that regulate synaptic structure and function. However, these processes are formed during embryonic or early postnatal development and it is unknown whether astrocytes can also ensheathe synapses of neurons born during adulthood and, if so, whether they play a role in their synaptic transmission. Here, we used a combination of serial-section immuno-electron microscopy, confocal microscopy, and electrophysiology to examine the formation of perisynaptic processes on adult-born neurons. We found that the afferent and efferent synapses of newborn neurons are ensheathed by astrocytic processes, irrespective of the age of the neurons or the size of their synapses. The quantification of gliogenesis and the distribution of astrocytic processes on synapses formed by adult-born neurons suggest that the majority of these processes are recruited from pre-existing astrocytes. Furthermore, the inhibition of astrocytic glutamate re-uptake significantly reduced postsynaptic currents and increased paired-pulse facilitation in adult-born neurons, suggesting that perisynaptic processes modulate synaptic transmission on these cells. Finally, some processes were found intercalated between newly formed dendritic spines and potential presynaptic partners, suggesting that they may also play a structural role in the connectivity of new spines. Together, these results indicate that pre-existing astrocytes remodel their processes to ensheathe synapses of adult-born neurons and participate to the functional and structural integration of these cells into the hippocampal network.
Fil: Krzisch, Marine. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Fil: Temprana, Silvio Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquimicas de Buenos Aires; Argentina. Fundación Instituto Leloir; Argentina
Fil: Mongiat, Lucas Alberto. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquimicas de Buenos Aires; Argentina. Fundación Instituto Leloir; Argentina
Fil: Armida, Jan. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Fil: Schmutz, Valentin. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Fil: Virtanen, Mari A.. Universidad de Ginebra; Suiza
Fil: Kocher Braissant, Jacqueline. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Fil: Kraftsik, Rudolf. University of Lausanne. Department of Fundamental Neurosciences; Suiza
Fil: Vutskits, Laszlo. Universidad de Ginebra; Suiza. University Hospital of Geneva. Department of Anesthesiology, Pharmacology and Intensive Care; Suiza
Fil: Conzelmann, Karl Klaus. Ludwig-Maximilians University Múnich. Max von Pettenkofer Institute and Gene Center; Alemania
Fil: Bergami, Matteo. University Hospital of Cologne; Alemania
Fil: Gage, Fred H.. Salk Institute for Biological Studies; Estados Unidos
Fil: Schinder, Alejandro Fabian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquimicas de Buenos Aires; Argentina. Fundación Instituto Leloir; Argentina
Fil: Toni, Nicolas. University of Lausanne. Department of Fundamental Neurosciences; Suiza
description The adult dentate gyrus produces new neurons that morphologically and functionally integrate into the hippocampal network. In the adult brain, most excitatory synapses are ensheathed by astrocytic perisynaptic processes that regulate synaptic structure and function. However, these processes are formed during embryonic or early postnatal development and it is unknown whether astrocytes can also ensheathe synapses of neurons born during adulthood and, if so, whether they play a role in their synaptic transmission. Here, we used a combination of serial-section immuno-electron microscopy, confocal microscopy, and electrophysiology to examine the formation of perisynaptic processes on adult-born neurons. We found that the afferent and efferent synapses of newborn neurons are ensheathed by astrocytic processes, irrespective of the age of the neurons or the size of their synapses. The quantification of gliogenesis and the distribution of astrocytic processes on synapses formed by adult-born neurons suggest that the majority of these processes are recruited from pre-existing astrocytes. Furthermore, the inhibition of astrocytic glutamate re-uptake significantly reduced postsynaptic currents and increased paired-pulse facilitation in adult-born neurons, suggesting that perisynaptic processes modulate synaptic transmission on these cells. Finally, some processes were found intercalated between newly formed dendritic spines and potential presynaptic partners, suggesting that they may also play a structural role in the connectivity of new spines. Together, these results indicate that pre-existing astrocytes remodel their processes to ensheathe synapses of adult-born neurons and participate to the functional and structural integration of these cells into the hippocampal network.
publishDate 2015
dc.date.none.fl_str_mv 2015-07
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/11336/9313
Krzisch, Marine; Temprana, Silvio Gabriel; Mongiat, Lucas Alberto; Armida, Jan; Schmutz, Valentin; et al.; Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus; Springer Heidelberg; Brain Structure & Function; 220; 4; 7-2015; 2027-2042
1863-2653
url http://hdl.handle.net/11336/9313
identifier_str_mv Krzisch, Marine; Temprana, Silvio Gabriel; Mongiat, Lucas Alberto; Armida, Jan; Schmutz, Valentin; et al.; Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus; Springer Heidelberg; Brain Structure & Function; 220; 4; 7-2015; 2027-2042
1863-2653
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://link.springer.com/article/10.1007%2Fs00429-014-0768-y
info:eu-repo/semantics/altIdentifier/doi/10.1007/s00429-014-0768-y
info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4481333/
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
application/pdf
dc.publisher.none.fl_str_mv Springer Heidelberg
publisher.none.fl_str_mv Springer Heidelberg
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 13.13397

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