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

ABSTRACT: 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.

SUBMITTER: Rauchs G

PROVIDER: S-EPMC2491899 | biostudies-literature | 2008

REPOSITORIES: biostudies-literature

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

Rauchs Géraldine G Orban Pierre P Schmidt Christina C Albouy Geneviève G Balteau Evelyne E Degueldre Christian C Schnackers Caroline C Sterpenich Virginie V Tinguely Gilberte G Luxen André A Maquet Pierre P Peigneux Philippe P

PloS one 20080813 8

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 re ...[more]

PMID: 18698363

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Project description:Successful consolidation of associative memories relies on the coordinated interplay of slow oscillations and sleep spindles during non-rapid eye movement (NREM) sleep. This enables the transfer of labile information from the hippocampus to permanent memory stores in the neocortex. During senescence, the decline of the structural and functional integrity of the hippocampus and neocortical regions is paralleled by changes of the physiological events that stabilize and enhance associative memories during NREM sleep. However, the currently available evidence is inconclusive as to whether and under which circumstances memory consolidation is impacted during aging. To approach this question, 30 younger adults (19-28 years) and 36 older adults (63-74 years) completed a memory task based on scene-word associations. By tracing the encoding quality of participants' individual memory associations, we demonstrate that previous learning determines the extent of age-related impairments in memory consolidation. Specifically, the detrimental effects of aging on memory maintenance were greatest for mnemonic contents of intermediate encoding quality, whereas memory gain of poorly encoded memories did not differ by age. Ambulatory polysomnography (PSG) and structural magnetic resonance imaging (MRI) data were acquired to extract potential predictors of memory consolidation from each participant's NREM sleep physiology and brain structure. Partial Least Squares Correlation was used to identify profiles of interdependent alterations in sleep physiology and brain structure that are characteristic for increasing age. Across age groups, both the 'aged' sleep profile, defined by decreased slow-wave activity (0.5-4.5 ?Hz), and a reduced presence of slow oscillations (0.5-1 ?Hz), slow, and fast spindles (9-12.5 ?Hz; 12.5-16 ?Hz), as well as the 'aged' brain structure profile, characterized by gray matter reductions in the medial prefrontal cortex, thalamus, entorhinal cortex, and hippocampus, were associated with reduced memory maintenance. However, inter-individual differences in neither sleep nor structural brain integrity alone qualified as the driving force behind age differences in sleep-dependent consolidation in the present study. Our results underscore the need for novel and age-fair analytic tools to provide a mechanistic understanding of age differences in memory consolidation.

Dataset Information

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

Publications

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

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