» Articles » PMID: 37080967

Hippocampal Sharp Wave Ripples Underlie Stress Susceptibility in Male Mice

Overview
Journal Nat Commun
Specialty Biology
Date 2023 Apr 20
PMID 37080967
Authors
Affiliations
Soon will be listed here.
Abstract

The ventral hippocampus (vHC) is a core brain region for emotional memory. Here, we examined how the vHC regulates stress susceptibility from the level of gene expression to neuronal population dynamics in male mice. Transcriptome analysis of samples from stress-naïve mice revealed that intrinsic calbindin (Calb1) expression in the vHC is associated with susceptibility to social defeat stress. Mice with Calb1 gene knockdown in the vHC exhibited increased stress resilience and failed to show the increase in the poststress ventral hippocampal sharp wave ripple (SWR) rate. Poststress vHC SWRs triggered synchronous reactivation of stress memory-encoding neuronal ensembles and facilitated information transfer to the amygdala. Suppression of poststress vHC SWRs by real-time feedback stimulation or walking prevented social behavior deficits. Taken together, our results demonstrate that internal reactivation of memories of negative stressful episodes supported by ventral hippocampal SWRs serves as a crucial neurophysiological substrate for determining stress susceptibility.

Citing Articles

Social and nonsocial environmental loss have differential effects on ventral hippocampus-dependent behavior and inhibitory synaptic markers in adult male mice.

Gore I, Brown C, Waters R, Gould E Learn Mem. 2024; 31(12).

PMID: 39681456 PMC: 11662144. DOI: 10.1101/lm.053968.124.


Luteolin ameliorates chronic stress-induced depressive-like behaviors in mice by promoting the Arginase-1 microglial phenotype via a PPARγ-dependent mechanism.

Yuan N, Zhu W, Ma Q, Huang M, Huo R, She K Acta Pharmacol Sin. 2024; 46(3):575-591.

PMID: 39496862 PMC: 11845711. DOI: 10.1038/s41401-024-01402-9.


Multivariate sharp-wave ripples in schizophrenia during awake state.

Ohki T, Chao Z, Takei Y, Kato Y, Sunaga M, Suto T Psychiatry Clin Neurosci. 2024; 78(9):507-516.

PMID: 38923051 PMC: 11488617. DOI: 10.1111/pcn.13702.


The defects of the hippocampal ripples and theta rhythm in depression, and the effects of physical exercise on their amelioration.

Koketsu S, Matsubara K, Ueki Y, Shinohara Y, Inoue K, Murakami S Heliyon. 2024; 10(1):e23738.

PMID: 38226277 PMC: 10788462. DOI: 10.1016/j.heliyon.2023.e23738.


Rescue of sharp wave-ripples and prevention of network hyperexcitability in the ventral but not the dorsal hippocampus of a rat model of fragile X syndrome.

Leontiadis L, Trompoukis G, Tsotsokou G, Miliou A, Felemegkas P, Papatheodoropoulos C Front Cell Neurosci. 2023; 17:1296235.

PMID: 38107412 PMC: 10722241. DOI: 10.3389/fncel.2023.1296235.

References
1.
Squire L, Genzel L, Wixted J, Morris R . Memory consolidation. Cold Spring Harb Perspect Biol. 2015; 7(8):a021766. PMC: 4526749. DOI: 10.1101/cshperspect.a021766. View

2.
Aurnhammer C, Haase M, Muether N, Hausl M, Rauschhuber C, Huber I . Universal real-time PCR for the detection and quantification of adeno-associated virus serotype 2-derived inverted terminal repeat sequences. Hum Gene Ther Methods. 2012; 23(1):18-28. DOI: 10.1089/hgtb.2011.034. View

3.
Tovote P, Fadok J, Luthi A . Neuronal circuits for fear and anxiety. Nat Rev Neurosci. 2015; 16(6):317-31. DOI: 10.1038/nrn3945. View

4.
Joo H, Frank L . The hippocampal sharp wave-ripple in memory retrieval for immediate use and consolidation. Nat Rev Neurosci. 2018; 19(12):744-757. PMC: 6794196. DOI: 10.1038/s41583-018-0077-1. View

5.
Zhang Y, Zhang X, Liu N, Ren S, Xia C, Yang X . Comparative Proteomic Characterization of Ventral Hippocampus in Susceptible and Resilient Rats Subjected to Chronic Unpredictable Stress. Front Neurosci. 2021; 15:675430. PMC: 8249003. DOI: 10.3389/fnins.2021.675430. View