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.
Highlights
Our understanding of the processes generating and maintaining sleep is rapidly increasing
We have found that hippocampal activity mostly supports spatial memory processes, whereas activity in parahippocampal, frontal, posterior parietal and lateral temporal cortices supports the contextual memory component [13]
In order to rule out the possibility of persisting effects of sleep deprivation at retesting, a psychomotor vigilance task (PVT) [20] was administered before learning and testing
Summary
Our understanding of the processes generating and maintaining sleep is rapidly increasing. Amongst the different functions that sleep may fulfill, lines of evidence gathered from cell recordings in rodents to behavioral and neuroimaging data in humans provide support to the idea that sleep participates in the long-term consolidation of recently acquired memories [1,2,3,4]. In this perspective, consolidation is defined as the process by which new memories are gradually transformed from an initially labile state (in which they are vulnerable to disruption) to a more permanent state in which they are stabilized and/or strengthened [1]. It was shown that learning-related brain activity is restructured during sleep in such a way that spatial navigation in a virtual environment, initially relying on a spatial-based, hippocampus-dependent strategy, becomes progressively contingent on a more automated response-based strategy mediated by the caudate nucleus [12]
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