Sleep modulates the neural substrates of both spatial and contextual memory consolidation.

It is known that sleep reshapes the neural representations that subtend the memories acquired while navigating in a virtual environment. However, navigation is not process-pure, as manifold learning components contribute to performance, notably the spatial and contextual memory constituents. In this...

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Autores principales: Géraldine Rauchs, Pierre Orban, Christina Schmidt, Geneviève Albouy, Evelyne Balteau, Christian Degueldre, Caroline Schnackers, Virginie Sterpenich, Gilberte Tinguely, André Luxen, Pierre Maquet, Philippe Peigneux
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Publicado: Public Library of Science (PLoS) 2008
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spelling oai:doaj.org-article:6b37533045044218af84d7b0c63af9312021-11-25T06:11:14ZSleep modulates the neural substrates of both spatial and contextual memory consolidation.1932-620310.1371/journal.pone.0002949https://doaj.org/article/6b37533045044218af84d7b0c63af9312008-08-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18698363/?tool=EBIhttps://doaj.org/toc/1932-6203It is known that sleep reshapes the neural representations that subtend the memories acquired while navigating in a virtual environment. However, navigation is not process-pure, as manifold learning components contribute to performance, notably the spatial and contextual memory constituents. In this context, it remains unclear whether post-training sleep globally promotes consolidation of all of the memory components embedded in virtual navigation, or rather favors the development of specific representations. Here, we investigated the effect of post-training sleep on the neural substrates of the consolidation of spatial and contextual memories acquired while navigating in a complex 3D, naturalistic virtual town. Using fMRI, we mapped regional cerebral activity during various tasks designed to tap either the spatial or the contextual memory component, or both, 72 h after encoding with or without sleep deprivation during the first post-training night. Behavioral performance was not dependent upon post-training sleep deprivation, neither in a natural setting that engages both spatial and contextual memory processes nor when looking more specifically at each of these memory representations. At the neuronal level however, analyses that focused on contextual memory revealed distinct correlations between performance and neuronal activity in frontal areas associated with recollection processes after post-training sleep, and in the parahippocampal gyrus associated with familiarity processes in sleep-deprived participants. Likewise, efficient spatial memory was associated with posterior cortical activity after sleep whereas it correlated with parahippocampal/medial temporal activity after sleep deprivation. Finally, variations in place-finding efficiency in a natural setting encompassing spatial and contextual elements were associated with caudate activity after post-training sleep, suggesting the automation of navigation. These data indicate that post-training sleep modulates the neural substrates of the consolidation of both the spatial and contextual memories acquired during virtual navigation.Géraldine RauchsPierre OrbanChristina SchmidtGeneviève AlbouyEvelyne BalteauChristian DegueldreCaroline SchnackersVirginie SterpenichGilberte TinguelyAndré LuxenPierre MaquetPhilippe PeigneuxPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 3, Iss 8, p e2949 (2008)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Géraldine Rauchs
Pierre Orban
Christina Schmidt
Geneviève Albouy
Evelyne Balteau
Christian Degueldre
Caroline Schnackers
Virginie Sterpenich
Gilberte Tinguely
André Luxen
Pierre Maquet
Philippe Peigneux
Sleep modulates the neural substrates of both spatial and contextual memory consolidation.
description It is known that sleep reshapes the neural representations that subtend the memories acquired while navigating in a virtual environment. However, navigation is not process-pure, as manifold learning components contribute to performance, notably the spatial and contextual memory constituents. In this context, it remains unclear whether post-training sleep globally promotes consolidation of all of the memory components embedded in virtual navigation, or rather favors the development of specific representations. Here, we investigated the effect of post-training sleep on the neural substrates of the consolidation of spatial and contextual memories acquired while navigating in a complex 3D, naturalistic virtual town. Using fMRI, we mapped regional cerebral activity during various tasks designed to tap either the spatial or the contextual memory component, or both, 72 h after encoding with or without sleep deprivation during the first post-training night. Behavioral performance was not dependent upon post-training sleep deprivation, neither in a natural setting that engages both spatial and contextual memory processes nor when looking more specifically at each of these memory representations. At the neuronal level however, analyses that focused on contextual memory revealed distinct correlations between performance and neuronal activity in frontal areas associated with recollection processes after post-training sleep, and in the parahippocampal gyrus associated with familiarity processes in sleep-deprived participants. Likewise, efficient spatial memory was associated with posterior cortical activity after sleep whereas it correlated with parahippocampal/medial temporal activity after sleep deprivation. Finally, variations in place-finding efficiency in a natural setting encompassing spatial and contextual elements were associated with caudate activity after post-training sleep, suggesting the automation of navigation. These data indicate that post-training sleep modulates the neural substrates of the consolidation of both the spatial and contextual memories acquired during virtual navigation.
format article
author Géraldine Rauchs
Pierre Orban
Christina Schmidt
Geneviève Albouy
Evelyne Balteau
Christian Degueldre
Caroline Schnackers
Virginie Sterpenich
Gilberte Tinguely
André Luxen
Pierre Maquet
Philippe Peigneux
author_facet Géraldine Rauchs
Pierre Orban
Christina Schmidt
Geneviève Albouy
Evelyne Balteau
Christian Degueldre
Caroline Schnackers
Virginie Sterpenich
Gilberte Tinguely
André Luxen
Pierre Maquet
Philippe Peigneux
author_sort Géraldine Rauchs
title Sleep modulates the neural substrates of both spatial and contextual memory consolidation.
title_short Sleep modulates the neural substrates of both spatial and contextual memory consolidation.
title_full Sleep modulates the neural substrates of both spatial and contextual memory consolidation.
title_fullStr Sleep modulates the neural substrates of both spatial and contextual memory consolidation.
title_full_unstemmed Sleep modulates the neural substrates of both spatial and contextual memory consolidation.
title_sort sleep modulates the neural substrates of both spatial and contextual memory consolidation.
publisher Public Library of Science (PLoS)
publishDate 2008
url https://doaj.org/article/6b37533045044218af84d7b0c63af931
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