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An Enduring Role for Hippocampal Pattern Completion in Addition to an Emergent Nonhippocampal Contribution to Holistic Episodic Retrieval after a 24 h Delay

Joensen, Bárður H. LU ; Ashton, Jennifer E. ; Berens, Sam C. ; Gareth Gaskell, M. and Horner, Aidan J. (2024) In Journal of Neuroscience 44(18).
Abstract

Episodic memory retrieval is associated with the holistic neocortical reinstatement of all event information, an effect driven by hippocampal pattern completion. However, whether holistic reinstatement occurs, and whether hippocampal pattern completion continues to drive reinstatement, after a period of consolidation is unclear. Theories of systems consolidation predict either a time-variant or time-invariant role of the hippocampus in the holistic retrieval of episodic events. Here, we assessed whether episodic events continue to be reinstated holistically and whether hippocampal pattern completion continues to facilitate holistic reinstatement following a period of consolidation. Female and male human participants learned “events”... (More)

Episodic memory retrieval is associated with the holistic neocortical reinstatement of all event information, an effect driven by hippocampal pattern completion. However, whether holistic reinstatement occurs, and whether hippocampal pattern completion continues to drive reinstatement, after a period of consolidation is unclear. Theories of systems consolidation predict either a time-variant or time-invariant role of the hippocampus in the holistic retrieval of episodic events. Here, we assessed whether episodic events continue to be reinstated holistically and whether hippocampal pattern completion continues to facilitate holistic reinstatement following a period of consolidation. Female and male human participants learned “events” that comprised multiple overlapping pairs of event elements (e.g., person–location, object–location, location–person). Importantly, encoding occurred either immediately before or 24 h before retrieval. Using fMRI during the retrieval of events, we show evidence for holistic reinstatement, as well as a correlation between reinstatement and hippocampal pattern completion, regardless of whether retrieval occurred immediately or 24 h after encoding. Thus, hippocampal pattern completion continues to contribute to holistic reinstatement after a delay. However, our results also revealed that some holistic reinstatement can occur without evidence for a corresponding signature of hippocampal pattern completion after a delay (but not immediately after encoding). We therefore show that hippocampal pattern completion, in addition to a nonhippocampal process, has a role in holistic reinstatement following a period of consolidation. Our results point to a consolidation process where the hippocampus and neocortex may work in an additive, rather than compensatory, manner to support episodic memory retrieval.

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author
; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
episodic memory, fMRI, hippocampus, systems consolidation
in
Journal of Neuroscience
volume
44
issue
18
article number
e1740232024
pages
12 pages
publisher
Society for Neuroscience
external identifiers
  • scopus:85192021268
  • pmid:38527810
ISSN
0270-6474
DOI
10.1523/JNEUROSCI.1740-23.2024
language
English
LU publication?
yes
additional info
Publisher Copyright: Copyright © 2024 Joensen et al.
id
7f0e2e38-d65b-470d-9997-6eed6db4432a
date added to LUP
2024-05-10 11:57:11
date last changed
2024-12-21 12:10:24
@article{7f0e2e38-d65b-470d-9997-6eed6db4432a,
  abstract     = {{<p>Episodic memory retrieval is associated with the holistic neocortical reinstatement of all event information, an effect driven by hippocampal pattern completion. However, whether holistic reinstatement occurs, and whether hippocampal pattern completion continues to drive reinstatement, after a period of consolidation is unclear. Theories of systems consolidation predict either a time-variant or time-invariant role of the hippocampus in the holistic retrieval of episodic events. Here, we assessed whether episodic events continue to be reinstated holistically and whether hippocampal pattern completion continues to facilitate holistic reinstatement following a period of consolidation. Female and male human participants learned “events” that comprised multiple overlapping pairs of event elements (e.g., person–location, object–location, location–person). Importantly, encoding occurred either immediately before or 24 h before retrieval. Using fMRI during the retrieval of events, we show evidence for holistic reinstatement, as well as a correlation between reinstatement and hippocampal pattern completion, regardless of whether retrieval occurred immediately or 24 h after encoding. Thus, hippocampal pattern completion continues to contribute to holistic reinstatement after a delay. However, our results also revealed that some holistic reinstatement can occur without evidence for a corresponding signature of hippocampal pattern completion after a delay (but not immediately after encoding). We therefore show that hippocampal pattern completion, in addition to a nonhippocampal process, has a role in holistic reinstatement following a period of consolidation. Our results point to a consolidation process where the hippocampus and neocortex may work in an additive, rather than compensatory, manner to support episodic memory retrieval.</p>}},
  author       = {{Joensen, Bárður H. and Ashton, Jennifer E. and Berens, Sam C. and Gareth Gaskell, M. and Horner, Aidan J.}},
  issn         = {{0270-6474}},
  keywords     = {{episodic memory; fMRI; hippocampus; systems consolidation}},
  language     = {{eng}},
  month        = {{05}},
  number       = {{18}},
  publisher    = {{Society for Neuroscience}},
  series       = {{Journal of Neuroscience}},
  title        = {{An Enduring Role for Hippocampal Pattern Completion in Addition to an Emergent Nonhippocampal Contribution to Holistic Episodic Retrieval after a 24 h Delay}},
  url          = {{http://dx.doi.org/10.1523/JNEUROSCI.1740-23.2024}},
  doi          = {{10.1523/JNEUROSCI.1740-23.2024}},
  volume       = {{44}},
  year         = {{2024}},
}