Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons

Autores
Sasaki, Takuya; Piatti, Veronica del Carmen; Hwaun, Ernie; Ahmadi, Siavash; Lisman, John E.; Leutgeb, Stefan; Leutgeb, Jill K.
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Complex spatial working memory tasks have been shown to require both hippocampal sharp-wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We therefore asked whether DG inputs to CA3 contribute to spatial working memory by promoting SWR generation. Recordings from DG and CA3 while rats performed a dentate-dependent working memory task on an eight-arm radial maze revealed that the activity of dentate neurons and the incidence rate of SWRs both increased during reward consumption. We then found reduced reward-related CA3 SWR generation without direct input from dentate granule neurons. Furthermore, CA3 cells with place fields in not-yet-visited arms preferentially fired during SWRs at reward locations, and these prospective CA3 firing patterns were more pronounced for correct trials and were dentate-dependent. These results indicate that coordination of CA3 neuronal activity patterns by DG is necessary for the generation of neuronal firing patterns that support goal-directed behavior and memory.
Fil: Sasaki, Takuya. University of California at San Diego; Estados Unidos. The University of Tokyo; Japón. Japan Science and Technology Agency; Japón
Fil: Piatti, Veronica del Carmen. University of California at San Diego; Estados Unidos
Fil: Hwaun, Ernie. University of California at San Diego; Estados Unidos
Fil: Ahmadi, Siavash. University of California at San Diego; Estados Unidos
Fil: Lisman, John E.. Brandeis University; Estados Unidos
Fil: Leutgeb, Stefan. University of California at San Diego; Estados Unidos
Fil: Leutgeb, Jill K.. University of California at San Diego; Estados Unidos
Materia
HIPPOCAMPUS
NEURAL CIRCUITS
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:11336/91142

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network_name_str CONICET Digital (CONICET)
spelling Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neuronsSasaki, TakuyaPiatti, Veronica del CarmenHwaun, ErnieAhmadi, SiavashLisman, John E.Leutgeb, StefanLeutgeb, Jill K.HIPPOCAMPUSNEURAL CIRCUITShttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3Complex spatial working memory tasks have been shown to require both hippocampal sharp-wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We therefore asked whether DG inputs to CA3 contribute to spatial working memory by promoting SWR generation. Recordings from DG and CA3 while rats performed a dentate-dependent working memory task on an eight-arm radial maze revealed that the activity of dentate neurons and the incidence rate of SWRs both increased during reward consumption. We then found reduced reward-related CA3 SWR generation without direct input from dentate granule neurons. Furthermore, CA3 cells with place fields in not-yet-visited arms preferentially fired during SWRs at reward locations, and these prospective CA3 firing patterns were more pronounced for correct trials and were dentate-dependent. These results indicate that coordination of CA3 neuronal activity patterns by DG is necessary for the generation of neuronal firing patterns that support goal-directed behavior and memory.Fil: Sasaki, Takuya. University of California at San Diego; Estados Unidos. The University of Tokyo; Japón. Japan Science and Technology Agency; JapónFil: Piatti, Veronica del Carmen. University of California at San Diego; Estados UnidosFil: Hwaun, Ernie. University of California at San Diego; Estados UnidosFil: Ahmadi, Siavash. University of California at San Diego; Estados UnidosFil: Lisman, John E.. Brandeis University; Estados UnidosFil: Leutgeb, Stefan. University of California at San Diego; Estados UnidosFil: Leutgeb, Jill K.. University of California at San Diego; Estados UnidosNature Publishing Group2018-02info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/91142Sasaki, Takuya; Piatti, Veronica del Carmen; Hwaun, Ernie; Ahmadi, Siavash; Lisman, John E.; et al.; Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons; Nature Publishing Group; Nature Neuroscience.; 21; 2; 2-2018; 258-2691097-6256CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1038/s41593-017-0061-5info:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41593-017-0061-5info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:20:29Zoai:ri.conicet.gov.ar:11336/91142instacron: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 10:20:29.539CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons
title Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons
spellingShingle Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons
Sasaki, Takuya
HIPPOCAMPUS
NEURAL CIRCUITS
title_short Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons
title_full Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons
title_fullStr Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons
title_full_unstemmed Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons
title_sort Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons
dc.creator.none.fl_str_mv Sasaki, Takuya
Piatti, Veronica del Carmen
Hwaun, Ernie
Ahmadi, Siavash
Lisman, John E.
Leutgeb, Stefan
Leutgeb, Jill K.
author Sasaki, Takuya
author_facet Sasaki, Takuya
Piatti, Veronica del Carmen
Hwaun, Ernie
Ahmadi, Siavash
Lisman, John E.
Leutgeb, Stefan
Leutgeb, Jill K.
author_role author
author2 Piatti, Veronica del Carmen
Hwaun, Ernie
Ahmadi, Siavash
Lisman, John E.
Leutgeb, Stefan
Leutgeb, Jill K.
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv HIPPOCAMPUS
NEURAL CIRCUITS
topic HIPPOCAMPUS
NEURAL CIRCUITS
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv Complex spatial working memory tasks have been shown to require both hippocampal sharp-wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We therefore asked whether DG inputs to CA3 contribute to spatial working memory by promoting SWR generation. Recordings from DG and CA3 while rats performed a dentate-dependent working memory task on an eight-arm radial maze revealed that the activity of dentate neurons and the incidence rate of SWRs both increased during reward consumption. We then found reduced reward-related CA3 SWR generation without direct input from dentate granule neurons. Furthermore, CA3 cells with place fields in not-yet-visited arms preferentially fired during SWRs at reward locations, and these prospective CA3 firing patterns were more pronounced for correct trials and were dentate-dependent. These results indicate that coordination of CA3 neuronal activity patterns by DG is necessary for the generation of neuronal firing patterns that support goal-directed behavior and memory.
Fil: Sasaki, Takuya. University of California at San Diego; Estados Unidos. The University of Tokyo; Japón. Japan Science and Technology Agency; Japón
Fil: Piatti, Veronica del Carmen. University of California at San Diego; Estados Unidos
Fil: Hwaun, Ernie. University of California at San Diego; Estados Unidos
Fil: Ahmadi, Siavash. University of California at San Diego; Estados Unidos
Fil: Lisman, John E.. Brandeis University; Estados Unidos
Fil: Leutgeb, Stefan. University of California at San Diego; Estados Unidos
Fil: Leutgeb, Jill K.. University of California at San Diego; Estados Unidos
description Complex spatial working memory tasks have been shown to require both hippocampal sharp-wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We therefore asked whether DG inputs to CA3 contribute to spatial working memory by promoting SWR generation. Recordings from DG and CA3 while rats performed a dentate-dependent working memory task on an eight-arm radial maze revealed that the activity of dentate neurons and the incidence rate of SWRs both increased during reward consumption. We then found reduced reward-related CA3 SWR generation without direct input from dentate granule neurons. Furthermore, CA3 cells with place fields in not-yet-visited arms preferentially fired during SWRs at reward locations, and these prospective CA3 firing patterns were more pronounced for correct trials and were dentate-dependent. These results indicate that coordination of CA3 neuronal activity patterns by DG is necessary for the generation of neuronal firing patterns that support goal-directed behavior and memory.
publishDate 2018
dc.date.none.fl_str_mv 2018-02
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/11336/91142
Sasaki, Takuya; Piatti, Veronica del Carmen; Hwaun, Ernie; Ahmadi, Siavash; Lisman, John E.; et al.; Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons; Nature Publishing Group; Nature Neuroscience.; 21; 2; 2-2018; 258-269
1097-6256
CONICET Digital
CONICET
url http://hdl.handle.net/11336/91142
identifier_str_mv Sasaki, Takuya; Piatti, Veronica del Carmen; Hwaun, Ernie; Ahmadi, Siavash; Lisman, John E.; et al.; Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons; Nature Publishing Group; Nature Neuroscience.; 21; 2; 2-2018; 258-269
1097-6256
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1038/s41593-017-0061-5
info:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41593-017-0061-5
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 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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