Sleep Spindles Promote the Restructuring of Memory Representations in Ventromedial Prefrontal Cortex through Enhanced Hippocampal-Cortical Functional Connectivity.


Journal

The Journal of neuroscience : the official journal of the Society for Neuroscience
ISSN: 1529-2401
Titre abrégé: J Neurosci
Pays: United States
ID NLM: 8102140

Informations de publication

Date de publication:
26 02 2020
Historique:
received: 08 08 2019
revised: 06 01 2020
accepted: 08 01 2020
pubmed: 22 1 2020
medline: 18 8 2020
entrez: 22 1 2020
Statut: ppublish

Résumé

Memory consolidation is hypothesized to involve the distribution and restructuring of memory representations across hippocampal and cortical regions. Theories suggest that, through extended hippocampal-cortical interactions, cortical ensembles come to represent more integrated, or overlapping, memory traces that prioritize commonalities across related memories. Sleep processes, particularly fast sleep spindles, are thought to support consolidation, but evidence for this relationship has been mostly limited to memory retention benefits. Whether fast spindles provide a mechanism for neural changes hypothesized to support consolidation, including the strengthening of hippocampal-cortical networks and integration across memory representations, remains unclear, as does the specificity of regions involved. Using functional connectivity analyses of human fMRI data (both sexes), we show that fast spindle density during overnight sleep is related to enhanced hippocampal-cortical functional connectivity the next day, when restudying information learned before sleep. Spindle density modulated connectivity in distinct hippocampal-cortical networks depending on the category of the consolidated stimuli. Specifically, spindle density correlated with functional connectivity between anterior hippocampus and ventromedial prefrontal cortex (vmPFC) for object-word pairs, and posterior hippocampus and posteromedial cortex for scene-word pairs. Using multivariate pattern analyses, we also show that fast spindle density during postlearning sleep is associated with greater pattern similarity, or representational overlap, across individual object-word memories in vmPFC the next day. Further, the relationship between fast spindle density and representational overlap in vmPFC was mediated by the degree of anterior hippocampal-vmPFC functional connectivity. Together, these results suggest that fast spindles support the network distribution of memory traces, potentially restructuring memory representations in vmPFC.

Identifiants

pubmed: 31959699
pii: JNEUROSCI.1946-19.2020
doi: 10.1523/JNEUROSCI.1946-19.2020
pmc: PMC7046449
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1909-1919

Subventions

Organisme : NINDS NIH HHS
ID : K23 NS104252
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH074692
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2020 the authors.

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Auteurs

Emily Cowan (E)

Center for Neural Science, New York University, New York, New York 10003.

Anli Liu (A)

Comprehensive Epilepsy Center, New York University, New York, New York 10016.
Department of Neurology, New York University Langone Health, New York, New York 10017.

Simon Henin (S)

Comprehensive Epilepsy Center, New York University, New York, New York 10016.
Department of Neurology, New York University Langone Health, New York, New York 10017.

Sanjeev Kothare (S)

Comprehensive Epilepsy Center, New York University, New York, New York 10016.
Department of Neurology, New York University Langone Health, New York, New York 10017.

Orrin Devinsky (O)

Comprehensive Epilepsy Center, New York University, New York, New York 10016.
Department of Neurology, New York University Langone Health, New York, New York 10017.

Lila Davachi (L)

Psychology Department, Columbia University, New York, New York 10027, and ld24@columbia.edu.
Nathan Kline Institute, Orangeburg, New York 10962.

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