Cited by 842Memory and Neural MechanismsSleep and Wakefulness ResearchMemory Processes and Influences

Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat

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Ego‐Stengel, Valérie, Wilson, Matthew A.·2010·Hippocampus

Abstract

The hippocampus plays a key role in the acquisition of new memories for places and events. Evidence suggests that the consolidation of these memories is enhanced during sleep. At the neuronal level, reactivation of awake experience in the hippocampus during sharp‐wave ripple events, characteristic of slow‐wave sleep, has been proposed as a neural mechanism for sleep‐dependent memory consolidation. However, a causal relation between sleep reactivation and memory consolidation has not been established. Here we show that disrupting neuronal activity during ripple events impairs spatial learning. We trained rats daily in two identical spatial navigation tasks followed each by a 1‐hour rest period. After one of the tasks, stimulation of hippocampal afferents selectively disrupted neuronal activity associated with ripple events without changing the sleep‐wake structure. Rats learned the control task significantly faster than the task followed by rest stimulation, indicating that interfering with hippocampal processing during sleep led to decreased learning. © 2009 Wiley‐Liss, Inc.

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Crossref · 10.1002/hipo.20707

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  • In rats, consolidation of hippocampus-dependent memories for a spatial maze was impaired following suppression of sharp-wave ripples typically accompanying memory reactivations during SWS.

    “In rats, consolidation of hippocampus-dependent memories for a spatial maze was impaired following suppression of sharp-wave ripples typically accompanying memory reactivations during SWS (Girardeau et al. 2009; Ego-Stengel & Wilson 2010).”

    From System consolidation of memory during sleep (2012) · cites this paper as Ego-Stengel & Wilson 2010

    The Abstract and Introduction report that disrupting ripple-associated hippocampal activity during post-task rest impaired rats’ spatial-maze learning. However, the Discussion says the study did not distinguish effects on ripples during slow-wave sleep from effects on ripples during wakefulness, so it cannot specifically attribute the impairment to suppression during SWS. Page numbers were not provided in our copy. (LLM, conf=0.86)

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  • In both studies, emergent ripple events were selectively disrupted by electrical stimulation during the rest period after learning, without disturbing sleep, which distinctly impaired consolidation of the acquired spatial memories.

    “In both studies, emergent ripple events were selectively disrupted by electrical stimulation during the rest period after learning, without disturbing sleep, which distinctly impaired consolidation of the acquired spatial memories.”

    From About Sleep's Role in Memory (2013) · cites this paper as [340]

  • Two recent studies in rats demonstrated a causal role of SW-Rs in memory consolidation.

    “Two recent studies in rats demonstrated a causal role of SW-Rs in memory consolidation (340, 458).”

    From About Sleep's Role in Memory (2013) · cites this paper as [340]

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Research works printed but not linked: 1

  1. Amaral DG Witter MP Paxinos G Hippocampal formation. The rat nervous system 1995 443 493 Academic Press San Diego Second ed.

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Authors
Ego‐Stengel, V., & Wilson, M. A.
Affiliations
  • Unit of Neuroscience Information and Complexity (FR)
  • Massachusetts Institute of Technology (US)
Corresponding author
Ego‐Stengel, Valérie
Venue
Hippocampus
Publisher
Wiley
Published
2009-10-08
Volume
20
Issue
1
Pages
1-10
ISSN
  • 1050-9631 (ISSN-L)
  • 1098-1063
OpenAlex
W2062205907
Cited by
842
References
43
Citations by year
2026: 46 · 2025: 54 · 2024: 58 · 2023: 57 · 2022: 69 · 2021: 49 · 2020: 54 · 2019: 75 · 2018: 67 · 2017: 62 · 2016: 53 · 2015: 44 · 2014: 42 · 2013: 39 · 2012: 34
FWCI
11.61
Type
journal article
Language
en
Open access
Locations
  • Hippocampus (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • HAL (submittedVersion)
  • DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
  • PubMed Central
Funders
  • Università della Calabria
  • National Institute of Mental Health (R01MH061976)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords
hippocampal ripples, sharp-wave ripples, sleep-dependent memory consolidation, spatial learning, slow-wave sleep, hippocampal reactivation, rest periods, spatial navigation
MeSH terms
Action Potentials, Afferent Pathways, Animals, Electric Stimulation, Electrodes, Implanted, Learning, Male, Neurons, Rest, Sleep, Space Perception, Time Factors, Pyramidal Cells, Maze Learning, Rats, Long-Evans, Rats, CA1 Region, Hippocampal

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