Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits

Autores
Boulanger Weill, Jonathan; Coste, Virginie; Jouary, Adrien; Romano, Sebastián Alejo; Pérez Schuster, Verónica; Sumbre, Germán
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
From development up to adulthood, the vertebrate brain is continuously supplied with newborn neurons that integrate into established mature circuits. However, how this process is coordinated during development remains unclear. Using two-photon imaging, GCaMP5 transgenic zebrafish larvae, and sparse electroporation in the larva's optic tectum, we monitored spontaneous and induced activity of large neuronal populations containing newborn and functionally mature neurons. We observed that the maturation of newborn neurons is a 4-day process. Initially, newborn neurons showed undeveloped dendritic arbors, no neurotransmitter identity, and were unresponsive to visual stimulation, although they displayed spontaneous calcium transients. Later on, newborn-labeled neurons began to respond to visual stimuli but in a very variable manner. At the end of the maturation period, newborn-labeled neurons exhibited visual tuning curves (spatial receptive fields and direction selectivity) and spontaneous correlated activity with neighboring functionally mature neurons. At this developmental stage, newborn-labeled neurons presented complex dendritic arbors and neurotransmitter identity (excitatory or inhibitory). Removal of retinal inputs significantly perturbed the integration of newborn neurons into the functionally mature tectal network. Our results provide a comprehensive description of the maturation of newborn neurons during development and shed light on potential mechanisms underlying their integration into a functionally mature neuronal circuit.
Fil: Boulanger Weill, Jonathan. Ecole Normale Supérieure; Francia
Fil: Coste, Virginie. Ecole Normale Supérieure; Francia
Fil: Jouary, Adrien. Ecole Normale Supérieure; Francia
Fil: Romano, Sebastián Alejo. Ecole Normale Supérieure; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigación en Biomedicina de Buenos Aires - Instituto Partner de la Sociedad Max Planck; Argentina
Fil: Pérez Schuster, Verónica. Ecole Normale Supérieure; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Física de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Física de Buenos Aires; Argentina
Fil: Sumbre, Germán. Ecole Normale Supérieure; Francia
Materia
NEUROGENESIS
NEWBORN NEURONS
OPTIC TECTUM
OPTOGENETICS
TWO-PHOTON CALCIUM IMAGING
VISUAL SYSTEM
ZEBRAFISH
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:11336/65309
Acceder
id CONICETDig_ef76d223349ce9920d28f7355de956f4
oai_identifier_str oai:ri.conicet.gov.ar:11336/65309
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal CircuitsBoulanger Weill, JonathanCoste, VirginieJouary, AdrienRomano, Sebastián AlejoPérez Schuster, VerónicaSumbre, GermánNEUROGENESISNEWBORN NEURONSOPTIC TECTUMOPTOGENETICSTWO-PHOTON CALCIUM IMAGINGVISUAL SYSTEMZEBRAFISHhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1From development up to adulthood, the vertebrate brain is continuously supplied with newborn neurons that integrate into established mature circuits. However, how this process is coordinated during development remains unclear. Using two-photon imaging, GCaMP5 transgenic zebrafish larvae, and sparse electroporation in the larva's optic tectum, we monitored spontaneous and induced activity of large neuronal populations containing newborn and functionally mature neurons. We observed that the maturation of newborn neurons is a 4-day process. Initially, newborn neurons showed undeveloped dendritic arbors, no neurotransmitter identity, and were unresponsive to visual stimulation, although they displayed spontaneous calcium transients. Later on, newborn-labeled neurons began to respond to visual stimuli but in a very variable manner. At the end of the maturation period, newborn-labeled neurons exhibited visual tuning curves (spatial receptive fields and direction selectivity) and spontaneous correlated activity with neighboring functionally mature neurons. At this developmental stage, newborn-labeled neurons presented complex dendritic arbors and neurotransmitter identity (excitatory or inhibitory). Removal of retinal inputs significantly perturbed the integration of newborn neurons into the functionally mature tectal network. Our results provide a comprehensive description of the maturation of newborn neurons during development and shed light on potential mechanisms underlying their integration into a functionally mature neuronal circuit.Fil: Boulanger Weill, Jonathan. Ecole Normale Supérieure; FranciaFil: Coste, Virginie. Ecole Normale Supérieure; FranciaFil: Jouary, Adrien. Ecole Normale Supérieure; FranciaFil: Romano, Sebastián Alejo. Ecole Normale Supérieure; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigación en Biomedicina de Buenos Aires - Instituto Partner de la Sociedad Max Planck; ArgentinaFil: Pérez Schuster, Verónica. Ecole Normale Supérieure; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Física de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Física de Buenos Aires; ArgentinaFil: Sumbre, Germán. Ecole Normale Supérieure; FranciaCell Press2017-06-19info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/65309Boulanger Weill, Jonathan; Coste, Virginie; Jouary, Adrien; Romano, Sebastián Alejo; Pérez Schuster, Verónica; et al.; Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits; Cell Press; Current Biology; 27; 12; 19-6-2017; 1707-1720.e50960-9822CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://www.sciencedirect.com/science/article/pii/S0960982217305651info:eu-repo/semantics/altIdentifier/doi/10.1016/j.cub.2017.05.029info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:27:38Zoai:ri.conicet.gov.ar:11336/65309instacron: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 10:27:38.658CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits
title Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits
spellingShingle Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits
Boulanger Weill, Jonathan
NEUROGENESIS
NEWBORN NEURONS
OPTIC TECTUM
OPTOGENETICS
TWO-PHOTON CALCIUM IMAGING
VISUAL SYSTEM
ZEBRAFISH
title_short Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits
title_full Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits
title_fullStr Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits
title_full_unstemmed Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits
title_sort Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits
dc.creator.none.fl_str_mv Boulanger Weill, Jonathan
Coste, Virginie
Jouary, Adrien
Romano, Sebastián Alejo
Pérez Schuster, Verónica
Sumbre, Germán
author Boulanger Weill, Jonathan
author_facet Boulanger Weill, Jonathan
Coste, Virginie
Jouary, Adrien
Romano, Sebastián Alejo
Pérez Schuster, Verónica
Sumbre, Germán
author_role author
author2 Coste, Virginie
Jouary, Adrien
Romano, Sebastián Alejo
Pérez Schuster, Verónica
Sumbre, Germán
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv NEUROGENESIS
NEWBORN NEURONS
OPTIC TECTUM
OPTOGENETICS
TWO-PHOTON CALCIUM IMAGING
VISUAL SYSTEM
ZEBRAFISH
topic NEUROGENESIS
NEWBORN NEURONS
OPTIC TECTUM
OPTOGENETICS
TWO-PHOTON CALCIUM IMAGING
VISUAL SYSTEM
ZEBRAFISH
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv From development up to adulthood, the vertebrate brain is continuously supplied with newborn neurons that integrate into established mature circuits. However, how this process is coordinated during development remains unclear. Using two-photon imaging, GCaMP5 transgenic zebrafish larvae, and sparse electroporation in the larva's optic tectum, we monitored spontaneous and induced activity of large neuronal populations containing newborn and functionally mature neurons. We observed that the maturation of newborn neurons is a 4-day process. Initially, newborn neurons showed undeveloped dendritic arbors, no neurotransmitter identity, and were unresponsive to visual stimulation, although they displayed spontaneous calcium transients. Later on, newborn-labeled neurons began to respond to visual stimuli but in a very variable manner. At the end of the maturation period, newborn-labeled neurons exhibited visual tuning curves (spatial receptive fields and direction selectivity) and spontaneous correlated activity with neighboring functionally mature neurons. At this developmental stage, newborn-labeled neurons presented complex dendritic arbors and neurotransmitter identity (excitatory or inhibitory). Removal of retinal inputs significantly perturbed the integration of newborn neurons into the functionally mature tectal network. Our results provide a comprehensive description of the maturation of newborn neurons during development and shed light on potential mechanisms underlying their integration into a functionally mature neuronal circuit.
Fil: Boulanger Weill, Jonathan. Ecole Normale Supérieure; Francia
Fil: Coste, Virginie. Ecole Normale Supérieure; Francia
Fil: Jouary, Adrien. Ecole Normale Supérieure; Francia
Fil: Romano, Sebastián Alejo. Ecole Normale Supérieure; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigación en Biomedicina de Buenos Aires - Instituto Partner de la Sociedad Max Planck; Argentina
Fil: Pérez Schuster, Verónica. Ecole Normale Supérieure; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Física de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Física de Buenos Aires; Argentina
Fil: Sumbre, Germán. Ecole Normale Supérieure; Francia
description From development up to adulthood, the vertebrate brain is continuously supplied with newborn neurons that integrate into established mature circuits. However, how this process is coordinated during development remains unclear. Using two-photon imaging, GCaMP5 transgenic zebrafish larvae, and sparse electroporation in the larva's optic tectum, we monitored spontaneous and induced activity of large neuronal populations containing newborn and functionally mature neurons. We observed that the maturation of newborn neurons is a 4-day process. Initially, newborn neurons showed undeveloped dendritic arbors, no neurotransmitter identity, and were unresponsive to visual stimulation, although they displayed spontaneous calcium transients. Later on, newborn-labeled neurons began to respond to visual stimuli but in a very variable manner. At the end of the maturation period, newborn-labeled neurons exhibited visual tuning curves (spatial receptive fields and direction selectivity) and spontaneous correlated activity with neighboring functionally mature neurons. At this developmental stage, newborn-labeled neurons presented complex dendritic arbors and neurotransmitter identity (excitatory or inhibitory). Removal of retinal inputs significantly perturbed the integration of newborn neurons into the functionally mature tectal network. Our results provide a comprehensive description of the maturation of newborn neurons during development and shed light on potential mechanisms underlying their integration into a functionally mature neuronal circuit.
publishDate 2017
dc.date.none.fl_str_mv 2017-06-19
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/11336/65309
Boulanger Weill, Jonathan; Coste, Virginie; Jouary, Adrien; Romano, Sebastián Alejo; Pérez Schuster, Verónica; et al.; Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits; Cell Press; Current Biology; 27; 12; 19-6-2017; 1707-1720.e5
0960-9822
CONICET Digital
CONICET
url http://hdl.handle.net/11336/65309
identifier_str_mv Boulanger Weill, Jonathan; Coste, Virginie; Jouary, Adrien; Romano, Sebastián Alejo; Pérez Schuster, Verónica; et al.; Functional Interactions between Newborn and Mature Neurons Leading to Integration into Established Neuronal Circuits; Cell Press; Current Biology; 27; 12; 19-6-2017; 1707-1720.e5
0960-9822
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://www.sciencedirect.com/science/article/pii/S0960982217305651
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.cub.2017.05.029
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 Cell Press
publisher.none.fl_str_mv Cell Press
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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