Abstract
Sleep strengthens memories by repeatedly reactivating associated neuron ensembles. Our studies show that although long-term memory for a medium number of word-pairs (160) benefits from sleep, a large number (320) does not. This suggests an upper limit to the amount of information that has access to sleep-dependent declarative memory consolidation, which is possibly linked to the availability of reactivation opportunities. Due to competing processes of global forgetting that are active during sleep, we hypothesized that even larger amounts of information would enhance the proportion of information that is actively forgotten during sleep. In the present study, we aimed to induce such forgetting by challenging the sleeping brain with vast amounts of to be remembered information. For this, 78 participants learned a very large number of 640 word-pairs interspersed with periods of quiet awake rest over the course of an entire day and then either slept or stayed awake during the night. Recall was tested after another night of regular sleep. Results revealed comparable retention rates between the sleep and wake groups. Although this null-effect can be reconciled with the concept of limited capacities available for sleep-dependent consolidation, it contradicts our hypothesis that sleep would increase forgetting compared to the wake group. Additional exploratory analyses relying on equivalence testing and Bayesian statistics reveal that there is evidence against sleep having a detrimental effect on the retention of declarative memory at high information loads. We argue that forgetting occurs in both wake and sleep states through different mechanisms, i.e., through increased interference and through global synaptic downscaling, respectively. Both of these processes might scale similarly with information load.
Highlights
MATERIALS AND METHODSIt is undisputed that sleep is integral to the formation of longterm memory (Diekelmann and Born, 2010; Walker and Stickgold, 2010; Rasch and Born, 2013; Klinzing et al, 2019)
The sleep and the wake group did not differ in retention performance on the word-pair task (MWake = −11.2 SEMWake = 1.73, MSleep = −8.5 SEMSleep = 1.70; sleep/wake: F1,74 = 1.25, p = 0.27; Figure 2)
Previous work suggests that sleep-dependent memory consolidation is a process limited in capacity and that learning large amounts of information overloads active systems consolidation and abolishes the positive effect of sleep on memory retention (Feld et al, 2016)
Summary
MATERIALS AND METHODSIt is undisputed that sleep is integral to the formation of longterm memory (Diekelmann and Born, 2010; Walker and Stickgold, 2010; Rasch and Born, 2013; Klinzing et al, 2019). Even though modern interpretations of this framework still exist, it is generally accepted that sleep plays an active role for memory (Ellenbogen et al, 2006b), with the two-stage model of memory formation (Marr, 1971; Diekelmann and Born, 2010; Rasch and Born, 2013; Klinzing et al, 2019) being the prevailing model used in declarative memory research. Reactivation of memory traces corresponds to sharp-wave/ripple events evident in the hippocampal local field potential recordings during sleep (Diba and Buzsáki, 2007) that coordinate with sleep spindles and sleep slow oscillations to drive active systems consolidation (Clemens et al, 2007; Staresina et al, 2015; Khodagholy et al, 2017). Sleep spindle density and reactivation in the form of sharp-wave/ripples have previously been shown to increase as a response to large amounts of learning material (Gais et al, 2002; Mölle et al, 2009), it is plausible that an active process of sleep on memory is limited by the amount of replay that can be accommodated
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