Publication Date

4-1-2024

Journal

Nature

DOI

10.1038/s41586-024-07192-8

PMID

38480889

PMCID

PMC11023929

PubMedCentral® Posted Date

3-13-2024

PubMedCentral® Full Text Version

Post-print

Published Open-Access

yes

Keywords

Animals, Mice, Hippocampus, Memory Consolidation, Arousal, Action Potentials, Neural Inhibition, Cognition, Brain Waves, Male, Female

Abstract

Distinct brain and behavioural states are associated with organized neural population dynamics that are thought to serve specific cognitive functions13. Memory replay events, for example, occur during synchronous population events called sharp-wave ripples in the hippocampus while mice are in an ‘offline’ behavioural state, enabling cognitive mechanisms such as memory consolidation and planning411. But how does the brain re-engage with the external world during this behavioural state and permit access to current sensory information or promote new memory formation? Here we found that the hippocampal dentate spike, an understudied population event that frequently occurs between sharp-wave ripples12, may underlie such a mechanism. We show that dentate spikes are associated with distinctly elevated brain-wide firing rates, primarily observed in higher order networks, and couple to brief periods of arousal. Hippocampal place coding during dentate spikes aligns to the mouse’s current spatial location, unlike the memory replay accompanying sharp-wave ripples. Furthermore, inhibiting neural activity during dentate spikes disrupts associative memory formation. Thus, dentate spikes represent a distinct brain state and support memory during non-locomotor behaviour, extending the repertoire of cognitive processes beyond the classical offline functions.

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