Abstract
While a role for sleep in declarative memory processing is established, the qualitative nature of this consolidation benefit, and the physiological mechanisms mediating it, remain debated. Here, we investigate the impact of sleep physiology on characteristics of episodic memory using an item- (memory elements) and context- (contextual details associated with those elements) learning paradigm; the latter being especially dependent on the hippocampus. Following back-to-back encoding of two word lists, each associated with a different context, participants were assigned to either a Nap-group, who obtained a 120-min nap, or a No Nap-group. Six hours post-encoding, participants performed a recognition test involving item-memory and context-memory judgments. In contrast to item-memory, which demonstrated no between-group differences, a significant benefit in context-memory developed in the Nap-group, the extent of which correlated both with the amount of stage-2 NREM sleep and frontal fast sleep-spindles. Furthermore, a difference was observed on the basis of word-list order, with the sleep benefit and associated physiological correlations being selective for the second word-list, learned last (most proximal to sleep). These findings suggest that sleep may preferentially benefit contextual (hippocampal-dependent) aspects of memory, supported by sleep-spindle oscillations, and that the temporal order of initial learning differentially determines subsequent offline consolidation.
Highlights
Substantive evidence indicates a proactive role for sleep in the consolidation of human declarative memory [1]
While a memory retention advantage was conferred by sleep relative to wake, this advantage was selective for the contextual qualitative features of the prior encoding episodic representations, rather than the basic item memory retention
Our findings demonstrate that (i) a short sleep period preferentially benefits more hippocampaldependent aspects of declarative memory representations, promoting superior retention of contextual episodic memory characteristics, relative to basic item-memory properties, (ii) these contextual memory benefits correlate with a particular stage of prior non-rapid eye movement (NREM) sleep, but a hallmark electrophysiological EEG oscillation of this sleep stage: fast sleep spindles, and (iii) this contextual memory advantage is dependent on the temporal order in which the initial information memory sets were encoded prior to sleep
Summary
Substantive evidence indicates a proactive role for sleep in the consolidation of human declarative memory [1]. Beyond sleep stages, associated NREM oscillations, including slow waves and sleep-spindle oscillations, continue to be implicated in the processing of declarative memories [8,9,10,11,12]. Sleepspindles, measured with surface electroencephalography (EEG), represent phasic oscillations commonly between 10–16 Hz, persisting for 1–3 s [7,13] Consistent with their proposed role in declarative memory, spindles are temporally linked, subcortically, with hippocampal sharp-wave ripple oscillations [1,14,15,16,17], which may play a causal role in consolidation and the transition from hippocampal to more neocortical memory dependence [18,19,20]. Sleep-spindles have further been separated into fast frequency (,13–15 Hz) and slow frequency (,11–13 Hz) subtypes [21,22], associated with unique functional anatomies, with faster sleep spindles being selectively associated with greater activity in, amongst other regions, the hippocampus [23]
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