The temporal origin of dentate granule neurons dictates their role in spatial memory.


Journal

Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835

Informations de publication

Date de publication:
12 2021
Historique:
received: 18 02 2021
revised: 20 07 2021
pubmed: 17 9 2021
medline: 15 3 2022
entrez: 16 9 2021
Statut: ppublish

Résumé

The dentate gyrus is one of the only brain regions that continues its development after birth in rodents. Adolescence is a very sensitive period during which cognitive competences are programmed. We investigated the role of dentate granule neurons (DGNs) born during adolescence in spatial memory and compared them with those generated earlier in life (in embryos or neonates) or during adulthood by combining functional imaging, retroviral and optogenetic tools to tag and silence DGNs. By imaging DGNs expressing Zif268, a proxy for neuronal activity, we found that neurons generated in adolescent rats (and not embryos or neonates) are transiently involved in spatial memory processing. In contrast, adult-generated DGNs are recruited at a later time point when animals are older. A causal relationship between the temporal origin of DGNs and spatial memory was confirmed by silencing DGNs in behaving animals. Our results demonstrate that the emergence of spatial memory depends on neurons born during adolescence, a function later assumed by neurons generated during adulthood.

Identifiants

pubmed: 34526669
doi: 10.1038/s41380-021-01276-x
pii: 10.1038/s41380-021-01276-x
pmc: PMC8873024
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

7130-7140

Informations de copyright

© 2021. The Author(s).

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Auteurs

Nuria Masachs (N)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Neurogenesis and Pathophysiology Group, U1215, F-33000, Bordeaux, France.

Vanessa Charrier (V)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Neurogenesis and Pathophysiology Group, U1215, F-33000, Bordeaux, France.

Fanny Farrugia (F)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Neurogenesis and Pathophysiology Group, U1215, F-33000, Bordeaux, France.

Valerie Lemaire (V)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Neurogenesis and Pathophysiology Group, U1215, F-33000, Bordeaux, France.

Nicolas Blin (N)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Neurogenesis and Pathophysiology Group, U1215, F-33000, Bordeaux, France.

Wilfrid Mazier (W)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Energy Balance and Obesity Group, U1215, F-33000, Bordeaux, France.

Sophie Tronel (S)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Neurogenesis and Pathophysiology Group, U1215, F-33000, Bordeaux, France.

Marie-Françoise Montaron (MF)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Neurogenesis and Pathophysiology Group, U1215, F-33000, Bordeaux, France.

Shaoyu Ge (S)

Program in Neuroscience, SUNY at Stony Brook, Stony Brook, New York, NY, USA.

Giovanni Marsicano (G)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Endocannabinoids and Neuroadaptation Group, U1215, F-33000, Bordeaux, France.

Daniela Cota (D)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Energy Balance and Obesity Group, U1215, F-33000, Bordeaux, France.

Véronique Deroche-Gamonet (V)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Psychobiology of Drug Addiction Group, U1215, F-33000, Bordeaux, France.

Cyril Herry (C)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Neuronal Circuits of Associative Learning Group, U1215, F-33000, Bordeaux, France.

Djoher Nora Abrous (DN)

Univ. Bordeaux, INSERM, Neurocenter Magendie, Neurogenesis and Pathophysiology Group, U1215, F-33000, Bordeaux, France. nora.abrous@inserm.fr.

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