Visual-area-specific tonic modulation of GABA release by endocannabinoids sets the activity and coordination of neocortical principal neurons
Perisomatic inhibition of pyramidal neurons (PNs) coordinates cortical network activity during sensory processing, and this role is mainly attributed to parvalbumin-expressing basket cells (BCs). However, cannabinoid receptor type 1 (CB1)-expressing interneurons are also BCs, but the connectivity an...
| Autores: | , , , , , , , , , , , , , , , |
|---|---|
| Tipo de recurso: | artículo |
| Estado: | Versión publicada |
| Fecha de publicación: | 2022 |
| País: | España |
| Institución: | Consejo Superior de Investigaciones Científicas (CSIC) |
| Repositorio: | DIGITAL.CSIC. Repositorio Institucional del CSIC |
| OAI Identifier: | oai:digital.csic.es:10261/284949 |
| Acceso en línea: | http://hdl.handle.net/10261/284949 |
| Access Level: | acceso abierto |
| Palabra clave: | CP: Neuroscience endocannabinoids Inhibition interneurons in vivo spontaneous activity synaptic transmission visual cortex. |
| id |
ES_87f8efa09600b0dcefffe9f7232e1d72 |
|---|---|
| oai_identifier_str |
oai:digital.csic.es:10261/284949 |
| network_acronym_str |
ES |
| network_name_str |
España |
| repository_id_str |
|
| spelling |
Visual-area-specific tonic modulation of GABA release by endocannabinoids sets the activity and coordination of neocortical principal neuronsKoukouli, F.Montmerle, M.Aguirre, A.De Brito Van Velze, M.Peixoto, J.Choudhary, V.Varilh, MarjorieJulio-Kalajzic, FranciscaAllene, C.Méndez, PabloZerlaut, Y.Marsicano, G.Schlüter, O.M.Rebola, NelsonBacci, AlbertoLourenço, J.CP: NeuroscienceendocannabinoidsInhibitioninterneuronsin vivo spontaneous activitysynaptic transmissionvisual cortex.Perisomatic inhibition of pyramidal neurons (PNs) coordinates cortical network activity during sensory processing, and this role is mainly attributed to parvalbumin-expressing basket cells (BCs). However, cannabinoid receptor type 1 (CB1)-expressing interneurons are also BCs, but the connectivity and function of these elusive but prominent neocortical inhibitory neurons are unclear. We find that their connectivity pattern is visual area specific. Persistently active CB1 signaling suppresses GABA release from CB1 BCs in the medial secondary visual cortex (V2M), but not in the primary visual cortex (V1). Accordingly, in vivo, tonic CB1 signaling is responsible for higher but less coordinated PN activity in the V2M than in the V1. These differential firing dynamics in the V1 and V2M can be captured by a computational network model that incorporates visual-area-specific properties. Our results indicate a differential CB1-mediated mechanism controlling PN activity, suggesting an alternative connectivity scheme of a specific GABAergic circuit in different cortical areas.We thank Brahim Abbes for providing the Fiji plugin (Neurostack) for soma colocalization analysis and quantification and Ronan Chéreau and Michael Graupner for initial help with 2P imaging implementation. We also thank members of the Bacci laboratory for helpful discussions and the ICM technical staff of the facilities PHENO-ICMICE, iGENSEQ, and Histomics. All animal work was conducted at the PHENO-ICMice facility. We gratefully acknowledge Joanna Droesbeke for performing part of the transcardial perfusions. F.K. thanks the Fondation des Treilles for awarding her the 2020 Young Re-searchers Prize. This work was supported by ‘‘Investissements d’avenir’’ ANR-10-IAIHU-06, Agence Nationale de la Recherche (ANR-13-BSV4-0015-01, ANR-16-CE16-0007-02, ANR-17-CE16-0026-01, ANR-18-CE16-0011-01, and ANR-20-CE16-0011-01), Fondation pour la Recherche Médicale (Equipes FRM – DEQ20150331684, Equipes FRM – EQU201903007860), DIM Region Ile de France, and a grant from the Institut du Cerveau et de la Moelle épiniére (Paris) (to A.B.); European Research Council starting grant 678250) and the Brain & Behavior Research Foundation (NARSAD Young Investigator Grant) (to N.R.); Fondation pour la Recherche Médicale (ARF 201909009117) (to Y.Z.); the German Research Foundation through the Cluster of Excellence (EXC2067) Multiscale Imaging and the Collaborative Research Center 889 (project B3) (to O.M.S.). The Core ICM facilities were supported by 2 ‘‘Investissements d’avenir’’ (ANR-10- IAIHU-06 and ANR-11-INBS-0011-NeurATRIS) and the ‘‘Fondation pour la Recherche Médicale’’. This project has received funding from the European Union’s Horizon 2020 research and innovation program under Marie Skłodowska-Curie grant agreement 892175 (to Y.Z.).Cell PressAgence Nationale de la Recherche (France)Fondation pour la Recherche MédicaleInstitut du Cerveau et de la Moelle Epinière (France)European Research CouncilEuropean CommissionConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2022202220222022info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/284949reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttp://dx.doi.org/10.1016/j.celrep.2022.111202Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2849492026-05-22T06:33:51Z |
| dc.title.none.fl_str_mv |
Visual-area-specific tonic modulation of GABA release by endocannabinoids sets the activity and coordination of neocortical principal neurons |
| title |
Visual-area-specific tonic modulation of GABA release by endocannabinoids sets the activity and coordination of neocortical principal neurons |
| spellingShingle |
Visual-area-specific tonic modulation of GABA release by endocannabinoids sets the activity and coordination of neocortical principal neurons Koukouli, F. CP: Neuroscience endocannabinoids Inhibition interneurons in vivo spontaneous activity synaptic transmission visual cortex. |
| title_short |
Visual-area-specific tonic modulation of GABA release by endocannabinoids sets the activity and coordination of neocortical principal neurons |
| title_full |
Visual-area-specific tonic modulation of GABA release by endocannabinoids sets the activity and coordination of neocortical principal neurons |
| title_fullStr |
Visual-area-specific tonic modulation of GABA release by endocannabinoids sets the activity and coordination of neocortical principal neurons |
| title_full_unstemmed |
Visual-area-specific tonic modulation of GABA release by endocannabinoids sets the activity and coordination of neocortical principal neurons |
| title_sort |
Visual-area-specific tonic modulation of GABA release by endocannabinoids sets the activity and coordination of neocortical principal neurons |
| dc.creator.none.fl_str_mv |
Koukouli, F. Montmerle, M. Aguirre, A. De Brito Van Velze, M. Peixoto, J. Choudhary, V. Varilh, Marjorie Julio-Kalajzic, Francisca Allene, C. Méndez, Pablo Zerlaut, Y. Marsicano, G. Schlüter, O.M. Rebola, Nelson Bacci, Alberto Lourenço, J. |
| author |
Koukouli, F. |
| author_facet |
Koukouli, F. Montmerle, M. Aguirre, A. De Brito Van Velze, M. Peixoto, J. Choudhary, V. Varilh, Marjorie Julio-Kalajzic, Francisca Allene, C. Méndez, Pablo Zerlaut, Y. Marsicano, G. Schlüter, O.M. Rebola, Nelson Bacci, Alberto Lourenço, J. |
| author_role |
author |
| author2 |
Montmerle, M. Aguirre, A. De Brito Van Velze, M. Peixoto, J. Choudhary, V. Varilh, Marjorie Julio-Kalajzic, Francisca Allene, C. Méndez, Pablo Zerlaut, Y. Marsicano, G. Schlüter, O.M. Rebola, Nelson Bacci, Alberto Lourenço, J. |
| author2_role |
author author author author author author author author author author author author author author author |
| dc.contributor.none.fl_str_mv |
Agence Nationale de la Recherche (France) Fondation pour la Recherche Médicale Institut du Cerveau et de la Moelle Epinière (France) European Research Council European Commission Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72] |
| dc.subject.none.fl_str_mv |
CP: Neuroscience endocannabinoids Inhibition interneurons in vivo spontaneous activity synaptic transmission visual cortex. |
| topic |
CP: Neuroscience endocannabinoids Inhibition interneurons in vivo spontaneous activity synaptic transmission visual cortex. |
| description |
Perisomatic inhibition of pyramidal neurons (PNs) coordinates cortical network activity during sensory processing, and this role is mainly attributed to parvalbumin-expressing basket cells (BCs). However, cannabinoid receptor type 1 (CB1)-expressing interneurons are also BCs, but the connectivity and function of these elusive but prominent neocortical inhibitory neurons are unclear. We find that their connectivity pattern is visual area specific. Persistently active CB1 signaling suppresses GABA release from CB1 BCs in the medial secondary visual cortex (V2M), but not in the primary visual cortex (V1). Accordingly, in vivo, tonic CB1 signaling is responsible for higher but less coordinated PN activity in the V2M than in the V1. These differential firing dynamics in the V1 and V2M can be captured by a computational network model that incorporates visual-area-specific properties. Our results indicate a differential CB1-mediated mechanism controlling PN activity, suggesting an alternative connectivity scheme of a specific GABAergic circuit in different cortical areas. |
| publishDate |
2022 |
| dc.date.none.fl_str_mv |
2022 2022 2022 2022 |
| dc.type.none.fl_str_mv |
info:eu-repo/semantics/article http://purl.org/coar/resource_type/c_6501 Publisher's version info:eu-repo/semantics/publishedVersion |
| format |
article |
| status_str |
publishedVersion |
| dc.identifier.none.fl_str_mv |
http://hdl.handle.net/10261/284949 |
| url |
http://hdl.handle.net/10261/284949 |
| dc.language.none.fl_str_mv |
Inglés |
| language_invalid_str_mv |
Inglés |
| dc.relation.none.fl_str_mv |
http://dx.doi.org/10.1016/j.celrep.2022.111202 Sí |
| dc.rights.none.fl_str_mv |
info:eu-repo/semantics/openAccess |
| eu_rights_str_mv |
openAccess |
| dc.publisher.none.fl_str_mv |
Cell Press |
| publisher.none.fl_str_mv |
Cell Press |
| dc.source.none.fl_str_mv |
reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC instname:Consejo Superior de Investigaciones Científicas (CSIC) |
| instname_str |
Consejo Superior de Investigaciones Científicas (CSIC) |
| reponame_str |
DIGITAL.CSIC. Repositorio Institucional del CSIC |
| collection |
DIGITAL.CSIC. Repositorio Institucional del CSIC |
| repository.name.fl_str_mv |
|
| repository.mail.fl_str_mv |
|
| _version_ |
1869412516021403649 |
| score |
15.811543 |