Abstract
Accumulating evidence emphasizes the relevance of oscillatory synchrony in memory consolidation during sleep. Sleep spindles promote memory retention, especially when occurring in the depolarized upstate of slow oscillation (SO). A less studied topic is the inter-spindle synchrony, i.e. the temporal overlap and phasic coherence between spindles perceived in different electroencephalography channels. In this study, we examined how synchrony between SOs and spindles, as well as between simultaneous spindles, is associated with the retention of novel verbal metaphors. Moreover, we combined the encoding of the metaphors with respiratory phase (inhalation/exhalation) with the aim of modulating the strength of memorized items, as previous studies have shown that inhalation entrains neural activity, thereby benefiting memory in a waking condition. In the current study, 27 young adults underwent a two-night mixed-design study with a 12-h delayed memory task during both sleep and waking conditions. As expected, we found better retention over the delay containing sleep, and this outcome was strongly associated with the timing of SO–spindle coupling. However, no associations were observed regarding inter-spindle synchrony or respiratory phase. These findings contribute to a better understanding of the importance of SO–spindle coupling for memory. In contrast, the observed lack of association with inter-spindle synchrony may emphasize the local nature of spindle-related plasticity.
Highlights
The benefits of sleep for memory retention have been widely acknowledged
Our main hypothesis was that we would observe a statistically significant positive association between memory retention over sleep conditions and the timing of slow oscillation (SO)–spindle coupling. We examined this phenomenon in non-rapid eye movement (NREM; N2 and N3 combined) sleep as well as separately for N2 and N3 stages; these stages potentially differ in coupling dynamics (Cox et al, 2018)
We found that one participant showed extremely high values for three SO–spindle coupling variables (>3 SD)
Summary
The benefits of sleep for memory retention have been widely acknowledged. Sleep protects memory function from wake–time interference and actively consolidates labile traces (Rasch and Born, 2013). Sleep spindles are considered biomarkers of sleep-related memory processing, promoting hippocampal–neocortical dialog (Ngo et al, 2020) and synaptic calcium-dependent plasticity processes (Peyrache and Seibt, 2020). Studies have frequently reported that the amount of spindles is associated with better memory outcomes after delay containing sleep (Gais et al, 2002; Clemens et al, 2005; Halonen et al, 2019). Sleep spindles do not occur in isolation. Recent research has stressed the importance of coordinated activity between cortical slow oscillations (SOs), sleep spindles, and hippocampal sharp-wave ripples with respect to facilitating active
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