Post-Training Sleep Modulates Topographical Relearning-Dependent Resting State Activity
Continuation of experience-dependent neural activity during offline sleep and wakefulness episodes is a critical component of memory consolidation. Using functional magnetic resonance imaging (fMRI), offline consolidation effects have been evidenced probing behavioural and neurophysiological changes...
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MDPI AG
2021-04-01
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Online Access: | https://www.mdpi.com/2076-3425/11/4/476 |
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author | Michele Deantoni Thomas Villemonteix Evelyne Balteau Christina Schmidt Philippe Peigneux |
author_facet | Michele Deantoni Thomas Villemonteix Evelyne Balteau Christina Schmidt Philippe Peigneux |
author_sort | Michele Deantoni |
collection | DOAJ |
description | Continuation of experience-dependent neural activity during offline sleep and wakefulness episodes is a critical component of memory consolidation. Using functional magnetic resonance imaging (fMRI), offline consolidation effects have been evidenced probing behavioural and neurophysiological changes during memory retrieval, i.e., in the context of task practice. Resting state fMRI (rsfMRI) further allows investigating the offline evolution of recently learned information without the confounds of online task-related effects. We used rsfMRI to investigate sleep-related changes in seed-based resting functional connectivity (FC) and amplitude of low frequency fluctuations (ALFF) after spatial navigation learning and relearning. On Day 1, offline resting state activity was measured immediately before and after topographical learning in a virtual town. On Day 4, it was measured again before and after relearning in an extended version of the town. Navigation-related activity was also recorded during target retrieval, i.e., online. Participants spent the first post-training night under regular sleep (RS) or sleep deprivation (SD) conditions. Results evidence FC and ALFF changes in task-related neural networks, indicating the continuation of navigation-related activity in the resting state. Although post-training sleep did not modulate behavioural performance, connectivity analyses evidenced increased FC after post-training SD between navigation-related brain structures during relearning in the extended environment. These results suggest that memory traces were less efficiently consolidated after post-learning SD, eventually resulting in the use of compensatory brain resources to link previously stored spatial elements with the newly presented information. |
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issn | 2076-3425 |
language | English |
last_indexed | 2024-03-10T12:28:41Z |
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spelling | doaj.art-1a2062db85234cc780b9d7d1a56efb8c2023-11-21T14:47:24ZengMDPI AGBrain Sciences2076-34252021-04-0111447610.3390/brainsci11040476Post-Training Sleep Modulates Topographical Relearning-Dependent Resting State ActivityMichele Deantoni0Thomas Villemonteix1Evelyne Balteau2Christina Schmidt3Philippe Peigneux4Neuropsychology and Functional Neuroimaging Research Unit (UR2NF) at CRCN—Centre for Research in Cognition and Neurosciences and UNI—ULB Neurosciences Institute, Université Libre de Bruxelles (ULB), CP191 Av. F. Roosevelt 50, 1050 Bruxelles, BelgiumNeuropsychology and Functional Neuroimaging Research Unit (UR2NF) at CRCN—Centre for Research in Cognition and Neurosciences and UNI—ULB Neurosciences Institute, Université Libre de Bruxelles (ULB), CP191 Av. F. Roosevelt 50, 1050 Bruxelles, BelgiumCRC-GIGA In Vivo Imaging, Université de Liège, Allée du 6 Août, Bâtiment B30, Sart Tilman, 4000 Liège, BelgiumCRC-GIGA In Vivo Imaging, Université de Liège, Allée du 6 Août, Bâtiment B30, Sart Tilman, 4000 Liège, BelgiumNeuropsychology and Functional Neuroimaging Research Unit (UR2NF) at CRCN—Centre for Research in Cognition and Neurosciences and UNI—ULB Neurosciences Institute, Université Libre de Bruxelles (ULB), CP191 Av. F. Roosevelt 50, 1050 Bruxelles, BelgiumContinuation of experience-dependent neural activity during offline sleep and wakefulness episodes is a critical component of memory consolidation. Using functional magnetic resonance imaging (fMRI), offline consolidation effects have been evidenced probing behavioural and neurophysiological changes during memory retrieval, i.e., in the context of task practice. Resting state fMRI (rsfMRI) further allows investigating the offline evolution of recently learned information without the confounds of online task-related effects. We used rsfMRI to investigate sleep-related changes in seed-based resting functional connectivity (FC) and amplitude of low frequency fluctuations (ALFF) after spatial navigation learning and relearning. On Day 1, offline resting state activity was measured immediately before and after topographical learning in a virtual town. On Day 4, it was measured again before and after relearning in an extended version of the town. Navigation-related activity was also recorded during target retrieval, i.e., online. Participants spent the first post-training night under regular sleep (RS) or sleep deprivation (SD) conditions. Results evidence FC and ALFF changes in task-related neural networks, indicating the continuation of navigation-related activity in the resting state. Although post-training sleep did not modulate behavioural performance, connectivity analyses evidenced increased FC after post-training SD between navigation-related brain structures during relearning in the extended environment. These results suggest that memory traces were less efficiently consolidated after post-learning SD, eventually resulting in the use of compensatory brain resources to link previously stored spatial elements with the newly presented information.https://www.mdpi.com/2076-3425/11/4/476functional MRIsleep deprivationmemory consolidationresting-state fMRIALFFspatial learning |
spellingShingle | Michele Deantoni Thomas Villemonteix Evelyne Balteau Christina Schmidt Philippe Peigneux Post-Training Sleep Modulates Topographical Relearning-Dependent Resting State Activity Brain Sciences functional MRI sleep deprivation memory consolidation resting-state fMRI ALFF spatial learning |
title | Post-Training Sleep Modulates Topographical Relearning-Dependent Resting State Activity |
title_full | Post-Training Sleep Modulates Topographical Relearning-Dependent Resting State Activity |
title_fullStr | Post-Training Sleep Modulates Topographical Relearning-Dependent Resting State Activity |
title_full_unstemmed | Post-Training Sleep Modulates Topographical Relearning-Dependent Resting State Activity |
title_short | Post-Training Sleep Modulates Topographical Relearning-Dependent Resting State Activity |
title_sort | post training sleep modulates topographical relearning dependent resting state activity |
topic | functional MRI sleep deprivation memory consolidation resting-state fMRI ALFF spatial learning |
url | https://www.mdpi.com/2076-3425/11/4/476 |
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