Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex

Autores
Gonzalez Burgos, Guillermo; Miyamae, Takeaki; Krimer, Yosef; Gulchina, Yelena; Pafundo, Diego Esteban; Krimer, Olga; Bazmi, Holly; Arion, Dominique; Enwright, John F.; Fish, Kenneth N.; Lewis, David A.
Año de publicación
2019
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
In primates, working memory function depends on activity in a distributed network of cortical areas that display different patterns of delay task-related activity. These differences are correlated with, and might depend on, distinctive properties of the neurons located in each area. For example, layer 3 pyramidal neurons (L3PNs) differ significantly between primary visual and dorsolateral prefrontal (DLPFC) cortices. However, to what extent L3PNs differ between DLPFC and other association cortical areas is less clear. Hence, we compared the properties of L3PNs in monkey DLPFC versus posterior parietal cortex (PPC), a key node in the cortical working memory network. Using patch-clamp recordings and biocytin cell filling in acute brain slices, we assessed the physiology and morphology of L3PNs from monkey DLPFC and PPC. The L3PN transcriptome was studied using laser microdissection combined with DNA microarray or quantitative PCR. We found that in both DLPFC and PPC, L3PNs were divided into regular spiking (RS-L3PNs) and bursting (B-L3PNs) physiological subtypes. Whereas regional differences in single-cell excitability were modest, B-L3PNs were rare in PPC (RS-L3PN:BL3PN, 94:6), but were abundant in DLPFC (50:50), showing greater physiological diversity. Moreover, DLPFC L3PNs display larger and more complex basal dendrites with higher dendritic spine density. Additionally, we found differential expression of hundreds of genes, suggesting a transcriptional basis for the differences in L3PN phenotype between DLPFC and PPC. These data show that the previously observed differences between DLPFC and PPC neuron activity during working memory tasks are associated with diversity in the cellular/ molecular properties of L3PNs.
Fil: Gonzalez Burgos, Guillermo. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Miyamae, Takeaki. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Krimer, Yosef. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Gulchina, Yelena. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Pafundo, Diego Esteban. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Krimer, Olga. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Bazmi, Holly. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Arion, Dominique. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Enwright, John F.. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Fish, Kenneth N.. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Lewis, David A.. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Materia
DENDRITES
LAYER 3
PARIETAL CORTEX
PFC
PYRAMIDAL NEURON
TRANSCRIPTOME
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:11336/120712
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/120712
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortexGonzalez Burgos, GuillermoMiyamae, TakeakiKrimer, YosefGulchina, YelenaPafundo, Diego EstebanKrimer, OlgaBazmi, HollyArion, DominiqueEnwright, John F.Fish, Kenneth N.Lewis, David A.DENDRITESLAYER 3PARIETAL CORTEXPFCPYRAMIDAL NEURONTRANSCRIPTOMEhttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3In primates, working memory function depends on activity in a distributed network of cortical areas that display different patterns of delay task-related activity. These differences are correlated with, and might depend on, distinctive properties of the neurons located in each area. For example, layer 3 pyramidal neurons (L3PNs) differ significantly between primary visual and dorsolateral prefrontal (DLPFC) cortices. However, to what extent L3PNs differ between DLPFC and other association cortical areas is less clear. Hence, we compared the properties of L3PNs in monkey DLPFC versus posterior parietal cortex (PPC), a key node in the cortical working memory network. Using patch-clamp recordings and biocytin cell filling in acute brain slices, we assessed the physiology and morphology of L3PNs from monkey DLPFC and PPC. The L3PN transcriptome was studied using laser microdissection combined with DNA microarray or quantitative PCR. We found that in both DLPFC and PPC, L3PNs were divided into regular spiking (RS-L3PNs) and bursting (B-L3PNs) physiological subtypes. Whereas regional differences in single-cell excitability were modest, B-L3PNs were rare in PPC (RS-L3PN:BL3PN, 94:6), but were abundant in DLPFC (50:50), showing greater physiological diversity. Moreover, DLPFC L3PNs display larger and more complex basal dendrites with higher dendritic spine density. Additionally, we found differential expression of hundreds of genes, suggesting a transcriptional basis for the differences in L3PN phenotype between DLPFC and PPC. These data show that the previously observed differences between DLPFC and PPC neuron activity during working memory tasks are associated with diversity in the cellular/ molecular properties of L3PNs.Fil: Gonzalez Burgos, Guillermo. Univeristy of Pittsburgh. School of Medicine; Estados UnidosFil: Miyamae, Takeaki. Univeristy of Pittsburgh. School of Medicine; Estados UnidosFil: Krimer, Yosef. Univeristy of Pittsburgh. School of Medicine; Estados UnidosFil: Gulchina, Yelena. Univeristy of Pittsburgh. School of Medicine; Estados UnidosFil: Pafundo, Diego Esteban. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; ArgentinaFil: Krimer, Olga. Univeristy of Pittsburgh. School of Medicine; Estados UnidosFil: Bazmi, Holly. Univeristy of Pittsburgh. School of Medicine; Estados UnidosFil: Arion, Dominique. Univeristy of Pittsburgh. School of Medicine; Estados UnidosFil: Enwright, John F.. Univeristy of Pittsburgh. School of Medicine; Estados UnidosFil: Fish, Kenneth N.. Univeristy of Pittsburgh. School of Medicine; Estados UnidosFil: Lewis, David A.. Univeristy of Pittsburgh. School of Medicine; Estados UnidosSociety for Neuroscience2019-07info: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/11336/120712Gonzalez Burgos, Guillermo; Miyamae, Takeaki; Krimer, Yosef; Gulchina, Yelena; Pafundo, Diego Esteban; et al.; Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex; Society for Neuroscience; Journal of Neuroscience; 39; 37; 7-2019; 7277-72900270-6474CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.jneurosci.org/content/early/2019/07/24/JNEUROSCI.1210-19.2019.longinfo:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.1210-19.2019info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:53:08Zoai:ri.conicet.gov.ar:11336/120712instacron: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 09:53:08.625CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex
title Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex
spellingShingle Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex
Gonzalez Burgos, Guillermo
DENDRITES
LAYER 3
PARIETAL CORTEX
PFC
PYRAMIDAL NEURON
TRANSCRIPTOME
title_short Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex
title_full Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex
title_fullStr Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex
title_full_unstemmed Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex
title_sort Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex
dc.creator.none.fl_str_mv Gonzalez Burgos, Guillermo
Miyamae, Takeaki
Krimer, Yosef
Gulchina, Yelena
Pafundo, Diego Esteban
Krimer, Olga
Bazmi, Holly
Arion, Dominique
Enwright, John F.
Fish, Kenneth N.
Lewis, David A.
author Gonzalez Burgos, Guillermo
author_facet Gonzalez Burgos, Guillermo
Miyamae, Takeaki
Krimer, Yosef
Gulchina, Yelena
Pafundo, Diego Esteban
Krimer, Olga
Bazmi, Holly
Arion, Dominique
Enwright, John F.
Fish, Kenneth N.
Lewis, David A.
author_role author
author2 Miyamae, Takeaki
Krimer, Yosef
Gulchina, Yelena
Pafundo, Diego Esteban
Krimer, Olga
Bazmi, Holly
Arion, Dominique
Enwright, John F.
Fish, Kenneth N.
Lewis, David A.
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv DENDRITES
LAYER 3
PARIETAL CORTEX
PFC
PYRAMIDAL NEURON
TRANSCRIPTOME
topic DENDRITES
LAYER 3
PARIETAL CORTEX
PFC
PYRAMIDAL NEURON
TRANSCRIPTOME
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv In primates, working memory function depends on activity in a distributed network of cortical areas that display different patterns of delay task-related activity. These differences are correlated with, and might depend on, distinctive properties of the neurons located in each area. For example, layer 3 pyramidal neurons (L3PNs) differ significantly between primary visual and dorsolateral prefrontal (DLPFC) cortices. However, to what extent L3PNs differ between DLPFC and other association cortical areas is less clear. Hence, we compared the properties of L3PNs in monkey DLPFC versus posterior parietal cortex (PPC), a key node in the cortical working memory network. Using patch-clamp recordings and biocytin cell filling in acute brain slices, we assessed the physiology and morphology of L3PNs from monkey DLPFC and PPC. The L3PN transcriptome was studied using laser microdissection combined with DNA microarray or quantitative PCR. We found that in both DLPFC and PPC, L3PNs were divided into regular spiking (RS-L3PNs) and bursting (B-L3PNs) physiological subtypes. Whereas regional differences in single-cell excitability were modest, B-L3PNs were rare in PPC (RS-L3PN:BL3PN, 94:6), but were abundant in DLPFC (50:50), showing greater physiological diversity. Moreover, DLPFC L3PNs display larger and more complex basal dendrites with higher dendritic spine density. Additionally, we found differential expression of hundreds of genes, suggesting a transcriptional basis for the differences in L3PN phenotype between DLPFC and PPC. These data show that the previously observed differences between DLPFC and PPC neuron activity during working memory tasks are associated with diversity in the cellular/ molecular properties of L3PNs.
Fil: Gonzalez Burgos, Guillermo. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Miyamae, Takeaki. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Krimer, Yosef. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Gulchina, Yelena. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Pafundo, Diego Esteban. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Krimer, Olga. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Bazmi, Holly. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Arion, Dominique. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Enwright, John F.. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Fish, Kenneth N.. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Lewis, David A.. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
description In primates, working memory function depends on activity in a distributed network of cortical areas that display different patterns of delay task-related activity. These differences are correlated with, and might depend on, distinctive properties of the neurons located in each area. For example, layer 3 pyramidal neurons (L3PNs) differ significantly between primary visual and dorsolateral prefrontal (DLPFC) cortices. However, to what extent L3PNs differ between DLPFC and other association cortical areas is less clear. Hence, we compared the properties of L3PNs in monkey DLPFC versus posterior parietal cortex (PPC), a key node in the cortical working memory network. Using patch-clamp recordings and biocytin cell filling in acute brain slices, we assessed the physiology and morphology of L3PNs from monkey DLPFC and PPC. The L3PN transcriptome was studied using laser microdissection combined with DNA microarray or quantitative PCR. We found that in both DLPFC and PPC, L3PNs were divided into regular spiking (RS-L3PNs) and bursting (B-L3PNs) physiological subtypes. Whereas regional differences in single-cell excitability were modest, B-L3PNs were rare in PPC (RS-L3PN:BL3PN, 94:6), but were abundant in DLPFC (50:50), showing greater physiological diversity. Moreover, DLPFC L3PNs display larger and more complex basal dendrites with higher dendritic spine density. Additionally, we found differential expression of hundreds of genes, suggesting a transcriptional basis for the differences in L3PN phenotype between DLPFC and PPC. These data show that the previously observed differences between DLPFC and PPC neuron activity during working memory tasks are associated with diversity in the cellular/ molecular properties of L3PNs.
publishDate 2019
dc.date.none.fl_str_mv 2019-07
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/11336/120712
Gonzalez Burgos, Guillermo; Miyamae, Takeaki; Krimer, Yosef; Gulchina, Yelena; Pafundo, Diego Esteban; et al.; Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex; Society for Neuroscience; Journal of Neuroscience; 39; 37; 7-2019; 7277-7290
0270-6474
CONICET Digital
CONICET
url http://hdl.handle.net/11336/120712
identifier_str_mv Gonzalez Burgos, Guillermo; Miyamae, Takeaki; Krimer, Yosef; Gulchina, Yelena; Pafundo, Diego Esteban; et al.; Distinct properties of layer 3 pyramidal neurons from prefrontal and parietal areas of the monkey neocortex; Society for Neuroscience; Journal of Neuroscience; 39; 37; 7-2019; 7277-7290
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/url/https://www.jneurosci.org/content/early/2019/07/24/JNEUROSCI.1210-19.2019.long
info:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.1210-19.2019
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 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

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