Post-Training Sleep Modulates Topographical Relearning-Dependent Resting State Activity

Abstract

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.

Total Sleep Deprivation Triggers Greater Activation in the Parietal Brain in the Visual Working Memory Updating Processes: An Event-Related Potentials Study

“…For instance, enhanced functional connectivity is reported within the ventral default mode network, as well as between two subsystems of the default mode network, which correlates with behavioral performance after TSD ( Chen et al, 2018 ). Functional connectivity between navigation-related brain structures increases during relearning in the extended environment after TSD, which represents the use of compensatory brain resources ( Deantoni et al, 2021 ). The increased functional connectivity between the thalamus and precuneus under TSD conditions is paralleled with greater recovery of working memory performance ( Yoo et al, 2007 ; Li et al, 2016 ).…”

Sleep-dependent structural neuroplasticity after a spatial navigation task: A diffusion imaging study

“…The navigation task is described in detail elsewhere (Deantoni et al, 2021), only essential information is reported here. Participants were trained in a previously used virtual navigation environment (Orban et al, 2006; Peigneux et al, 2006; Rauchs, Orban, Balteau, et al, 2008), that features a complex town made of two levels communicating through two teleports (Figure 1).…”

“…At the end of the four 8-minute blocks of free exploration, participants are exposed to 10 test trials in a row to estimate their navigation performance. A quantitative performance measure is computed for each trial as the shortest distance remaining between the subject’s actual location at the end of the trial time limit and the location of the target destination, based on video screen recordings of their navigation (Deantoni et al, 2021; Orban et al, 2006; Peigneux et al, 2006; Rauchs, Orban, Balteau, et al, 2008). Participants were also tested on 10 L1 navigation trials during a fMRI session on Day 1 after learning before DWI-2 and on Day 4 before relearning after DWI-3.…”

“…For task-based fMRI, multi-slice T2*-weighted functional images were acquired with a gradient-echo echo-planar imaging EPI) sequence using axial slice orientation and covering the whole brain (36 slices, FoV = 216 × 216 mm2, voxel size 3 × 3 × 3 mm3, 25% interslice gap, matrix size = 72 × 72 × 36, repetition time (TR) = 2260 ms, echo time (TE) = 30 ms, flip angle (FA) = 90 deg). Processing and analyses of task-based fMRI data are reported in Deantoni et al (2021).…”

Capturing early human memory consolidation utilizing the higher functional specificity of 7T compared to 3T-fMRI

“…Occurrence and strength, especially of hippocampal replay patterns, were correlated with subsequent memory performance 15,16 . Similarly, two human 3T-fMRI studies investigated whether FC-modulation in the resting-state was associated with a previous declarative learning task 17,18 . Although these studies detected a few modulated connections in predefined regions activated during encoding, these were not correlated with memory performance and not controlled for the natural variation of the participant’s resting-state between consecutive measurements.…”