The gut-brain vagal axis scales hippocampal memory processes and plasticity

Author: Oriane Onimus1, Faustine Arrivet2, Isis Nem de Oliveira Souza3, Benoit Bertrand1, Julien Castel1, Serge Luquet1, Jean-Pierre Mothet4, Nicolas Heck2, Giuseppe Gangarossa5
Affiliation:
1 Université Paris Cité, CNRS, Unité de Biologie Fonctionnelle et Adaptative, F-75013 Paris, France.
2 Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine, Institut de Biologie Paris Seine, F-75005 Paris, France.
3 Biophotonics and Synapse Physiopathology Team, Laboratoire LuMIn UMR9024 Université Paris-Saclay, ENS Paris-Saclay, CNRS, CentraleSupelec, 91190 Gif-sur-Yvette, France; Laboratory of Molecular Pharmacology, Institute of Biomedical Sciences, Universidade Federal do Rio de Janeiro, Brazil.
4 Biophotonics and Synapse Physiopathology Team, Laboratoire LuMIn UMR9024 Université Paris-Saclay, ENS Paris-Saclay, CNRS, CentraleSupelec, 91190 Gif-sur-Yvette, France.
5 Université Paris Cité, CNRS, Unité de Biologie Fonctionnelle et Adaptative, F-75013 Paris, France; Institut Universitaire de France, France. Electronic address: giuseppe.gangarossa@u-paris.fr.
Conference/Journal: Neurobiol Dis
Date published: 2024 Jun 15
Other: Pages: 106569 , Special Notes: doi: 10.1016/j.nbd.2024.106569. , Word Count: 224


The vagus nerve serves as an interoceptive relay between the body and the brain. Despite its well-established role in feeding behaviors, energy metabolism, and cognitive functions, the intricate functional processes linking the vagus nerve to the hippocampus and its contribution to learning and memory dynamics remain still elusive. Here, we investigated whether and how the gut-brain vagal axis contributes to hippocampal learning and memory processes at behavioral, functional, cellular, and molecular levels. Our results indicate that the integrity of the vagal axis is essential for long-term recognition memories, while sparing other forms of memory. In addition, by combing multi-scale approaches, our findings show that the gut-brain vagal tone exerts a permissive role in scaling intracellular signaling events, gene expressions, hippocampal dendritic spines density as well as functional long-term plasticities (LTD and LTP). These results highlight the critical role of the gut-brain vagal axis in maintaining the spontaneous and homeostatic functions of hippocampal ensembles and in regulating their learning and memory functions. In conclusion, our study provides comprehensive insights into the multifaceted involvement of the gut-brain vagal axis in shaping time-dependent hippocampal learning and memory dynamics. Understanding the mechanisms underlying this interoceptive body-brain neuronal communication may pave the way for novel therapeutic approaches in conditions associated with cognitive decline, including neurodegenerative disorders.

Keywords: Gut-brain axis; Learning and memory; Vagus nerve; hippocampus.

PMID: 38885849 DOI: 10.1016/j.nbd.2024.106569

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