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Dentate Gyrus Sharp Waves, a Local Field Potential Correlate of Learning in the Dentate Gyrus of Mice.

Authors
  • Meier, Kolja1, 2
  • Merseburg, Andrea2, 3
  • Isbrandt, Dirk4, 3
  • Marguet, Stephan Lawrence2, 3
  • Morellini, Fabio1
  • 1 Behavioral Biology, Center for Molecular Neurobiology, University Medical Center Hamburg-Eppendorf, Hamburg 20251, Germany. , (Germany)
  • 2 German Center for Neurodegenerative Diseases (DZNE), Bonn 53175, Germany. , (Germany)
  • 3 Institute for Molecular and Behavioral Neuroscience, Faculty of Medicine, University of Cologne, Cologne 50937, Germany. , (Germany)
  • 4 German Center for Neurodegenerative Diseases (DZNE), Bonn 53175, Germany [email protected] , (Germany)
Type
Published Article
Journal
Journal of Neuroscience
Publisher
Society for Neuroscience
Publication Date
Sep 09, 2020
Volume
40
Issue
37
Pages
7105–7118
Identifiers
DOI: 10.1523/JNEUROSCI.2275-19.2020
PMID: 32817247
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

The hippocampus plays an essential role in learning. Each of the three major hippocampal subfields, dentate gyrus (DG), CA3, and CA1, has a unique function in memory formation and consolidation, and also exhibit distinct local field potential (LFP) signatures during memory consolidation processes in non-rapid eye movement (NREM) sleep. The classic LFP events of the CA1 region, sharp-wave ripples (SWRs), are induced by CA3 activity and considered to be an electrophysiological biomarker for episodic memory. In LFP recordings along the dorsal CA1-DG axis from sleeping male mice, we detected and classified two types of LFP events in the DG: high-amplitude dentate spikes (DSs), and a novel event type whose current source density (CSD) signature resembled that seen during CA1 SWR, but which, most often, occurred independently of them. Because we hypothesize that this event type is similarly induced by CA3 activity, we refer to it as dentate sharp wave (DSW). We show that both DSWs and DSs differentially modulate the electrophysiological properties of SWR and multiunit activity (MUA). Following two hippocampus-dependent memory tasks, DSW occurrence rates, ripple frequencies, and ripple and sharp wave (SW) amplitudes were increased in both, while SWR occurrence rates in dorsal CA1 increased only after the spatial task. Our results suggest that DSWs, like SWRs, are induced by CA3 activity and that DSWs complement SWRs as a hippocampal LFP biomarker of memory consolidation.SIGNIFICANCE STATEMENT Awake experience is consolidated into long-term memories during sleep. Memory consolidation crucially depends on sharp-wave ripples (SWRs), which are local field potential (LFP) patterns in hippocampal CA1 that increase after learning. The dentate gyrus (DG) plays a central role in the process of memory formation, prompting us to cluster sharp waves (SWs) in the DG [dentate SWs (DSWs)] during sleep. We show that both DSW coupling to CA1 SWRs, and their occurrence rates, robustly increase after learning trials. Our results suggest that the DG is directly affected by memory consolidation processes. DSWs may thus complement SWRs as a sensitive electrophysiological biomarker of memory consolidation in mice. Copyright © 2020 the authors.

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