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Microbiota and stress: a loop that impacts memory

Authors :
Olivier Zemb
Sylvie Rabot
Hugues Dardente
Céline Parias
Florent Kempf
Anaïs Vitorino Carvalho
Catherine Philippe
Thierry Chaumeil
Marie-Pierre Moisan
Vincent Coustham
Philippe Velge
Aline Foury
Ludovic Calandreau
Narjis Kraimi
Julie Lemarchand
Karine Germain
Christine Leterrier
Flore Lormant
Paul Constantin
Physiologie de la reproduction et des comportements [Nouzilly] (PRC)
Institut Français du Cheval et de l'Equitation [Saumur]-Université de Tours-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Infectiologie et Santé Publique (UMR ISP)
Université de Tours-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Génétique Physiologie et Systèmes d'Elevage (GenPhySE )
Ecole Nationale Vétérinaire de Toulouse (ENVT)
Institut National Polytechnique (Toulouse) (Toulouse INP)
Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP)
Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-École nationale supérieure agronomique de Toulouse [ENSAT]-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Elevage Alternatif et Santé des Monogastriques (UE EASM)
Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
MICrobiologie de l'ALImentation au Service de la Santé (MICALIS)
AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Nutrition et Neurobiologie intégrée (NutriNeuro)
Université de Bordeaux (UB)-Institut Polytechnique de Bordeaux-Ecole nationale supérieure de chimie, biologie et physique-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Biologie des Oiseaux et Aviculture (BOA)
Plateforme d'Infectiologie Expérimentale (PFIE)
Institut Français du Cheval et de l'Equitation [Saumur]-Université de Tours (UT)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Université de Tours (UT)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Source :
Psychoneuroendocrinology, Psychoneuroendocrinology, Elsevier, 2022, ⟨10.1016/j.psyneuen.2021.105594⟩
Publication Year :
2021

Abstract

Chronic stress and the gut microbiota appear to comprise a feed-forward loop, which contributes to the development of depressive disorders. Evidence suggests that memory can also be impaired by either chronic stress or microbiota imbalance. However, it remains to be established whether these could be a part of an integrated loop model and be responsible for memory impairments. To shed light on this, we used a two-pronged approach in Japanese quail: first stress-induced alterations in gut microbiota were characterized, then we tested whether this altered microbiota could affect brain and memory function when transferred to a germ-free host. The cecal microbiota of chronically stressed quails was found to be significantly different from that of unstressed individuals with lower α and β diversities and increased Bacteroidetes abundance largely represented by the Alistipes genus, a well-known stress target in rodents and humans. The transfer of this altered microbiota into germ-free quails decreased their spatial and cue-based memory abilities as previously demonstrated in the stressed donors. The recipients also displayed increased anxiety-like behavior, reduced basal plasma corticosterone levels and differential gene expression in the brain. Furthermore, cecal microbiota transfer from a chronically stressed individual was sufficient to mimic the adverse impact of chronic stress on memory in recipient hosts and this action may be related to the Alistipes genus. Our results provide evidence of a feed-forward loop system linking the microbiota-gut-brain axis to stress and memory function and suggest that maintaining a healthy microbiota could help alleviate memory impairments linked to chronic stress. Availability of data and materials The datasets used during the current study are available from the corresponding author on reasonable request and they are available at https://doi.org/10.15454/JYITK4 .

Details

ISSN :
18733360 and 03064530
Volume :
136
Database :
OpenAIRE
Journal :
Psychoneuroendocrinology
Accession number :
edsair.doi.dedup.....f77b3949493c0c4b36730ef008ec5dff
Full Text :
https://doi.org/10.1016/j.psyneuen.2021.105594⟩