Cited by 276Memory and Neural MechanismsMemory Processes and InfluencesSleep and Wakefulness Research

Shift from hippocampal to neocortical centered retrieval network with consolidation

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Takashima, Atsuko, Nieuwenhuis, Ingrid L.C., Jensen, Ole, Talamini, Lucia M., Rijpkema, Mark, Fernández, Guillén·2009·The Journal of Neuroscience

Abstract

The standard model of system-level consolidation posits that the hippocampus is part of a retrieval network for recent memories. According to this theory, the memories are gradually transferred to neocortical circuits with consolidation, where the connections within this circuit grow stronger and reorganized so that redundant and/or contextual details may be lost. Thus, remote memories are based on neocortical networks and can be retrieved independently of the hippocampus. To test this model, we measured regional brain activity and connectivity during retrieval with functional magnetic resonance imaging. Subjects were trained on two sets of face-location association and were tested with two different delays, 15 min and 24 h including a whole night of sleep. We hypothesized that memory traces of the locations associated with specific faces will be linked through the hippocampus for the retrieval of recently learned association, but with consolidation, the activity and the functional connectivity between the neocortical areas will increase. We show that posterior hippocampal activity related to high-confidence retrieval decreased and neocortical activity increased with consolidation. Moreover, the connectivity between the hippocampus and the neocortical regions decreased and in turn, cortico-cortical connectivity between the representational areas increased. The results provide mechanistic support for a two-level process of the declarative memory system, involving initial representation of new associations in a network including the hippocampus and subsequent consolidation into a predominantly neocortical network.

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Crossref · 10.1523/jneurosci.0799-09.2009

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  • One night of sleep decreases hippocampal activation and increases activation in neocortex areas.

    “A second study of this group confirmed that one night of sleep decreases hippocampal activation and increases activation in neocortex areas (1169).”

    From About Sleep's Role in Memory (2013) · cites this paper as [1169]

    The Discussion reports lower posterior hippocampal activity and higher activity in neocortical representational areas with consolidation over a night of sleep. The study compared retrieval after 15 minutes with retrieval after 24 hours including sleep; it does not establish that sleep itself, rather than the intervening consolidation period, caused the changes. (LLM, conf=0.82)

    Experimental — accuracy not yet measured
  • Differences in the posterior HF have been commonly observed for studies using associative memory tasks.

    “differences in the posterior HF have been commonly observed for studies using associative memory tasks”
  • Studies that isolated activity for high-confidence, recollection-based or associative hits have often reported delay-dependence.

    “studies that isolated activity for high-confidence, recollection-based or associative hits have often reported delay-dependence”

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Authors
Takashima, A., Nieuwenhuis, I. L. C., Jensen, O., Talamini, L. M., Rijpkema, M., & Fernández, G.
Affiliations
  • Radboud University Nijmegen (NL)
  • University of Amsterdam (NL)
Venue
The Journal of Neuroscience
Published
2009-08-12
Volume
29
Issue
32
Pages
10087-10093
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2023544141
Cited by
276
References
58
Citations by year
2026: 6 · 2025: 15 · 2024: 17 · 2023: 12 · 2022: 13 · 2021: 11 · 2020: 16 · 2019: 15 · 2018: 20 · 2017: 19 · 2016: 24 · 2015: 18 · 2014: 16 · 2013: 17 · 2012: 18
FWCI
9.23
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • UvA-DARE (University of Amsterdam) (submittedVersion)
  • Radboud Repository (Radboud University) (submittedVersion)
  • Radboud Repository (Radboud University) (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (051-04-100)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Keywords
memory consolidation, hippocampus, neocortex, memory retrieval, declarative memory, corticocortical connections, sleep, memory confidence
MeSH terms
Adult, Association Learning, Brain Mapping, Cerebral Cortex, Face, Female, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Memory, Memory, Short-Term, Neural Pathways, Photic Stimulation, Reaction Time, Sleep, Space Perception, Time Factors, Visual Perception

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