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Introduction: The sequence of cortical down-states, up-states, and spindle events provides a core electrophysiological basis for memory consolidation during non-REM sleep. However, the mechanisms orchestrating this coordination remain elusive. Here, we applied phase-targeted auditory stimulation (PTAS) at slow oscillation (SO) phases of maximal excitability or inhibition to identify spectral signatures underlying slow wave generation and coordination with spindles. We also compared stimulus-evoked slow waves, spontaneous SOs, and K-complexes to determine a shared spectral fingerprint supporting spindle synchronization.
Methods: Twenty-six participants (23.23±2.61 years, 17 females) slept at home wearing an EEG headband (Fpz-M1, AF8-M1) coupled with an algorithm delivering 50-msec pink noises (45 dB) during SO up- and down-states. EEG responses were analyzed through event-related potentials (ERPs) and event-related spectral perturbations. Furthermore, slow waves were detected post hoc throughout the night and categorized as stimulus-evoked, spontaneous SOs (N3), or K-complexes (N2).
Results: PTAS-up elicited larger negative and positive peaks at ~500 and ~1000 msec, greater pre-down-state theta activity (5-8 Hz), and stronger up-state-coupled spindle power (12-16 Hz) than PTAS-down (all p<0.001). Theta response robustly predicted ERP amplitude and spindle power (both r=0.70).
Stimulus-evoked events and K-complexes shared overlapping spectral profiles with higher pre-down-state theta and up-state-coupled spindle activity than spontaneous SOs (all p<0.001). Early theta strongly predicted spindle activity across all categories (r=0.78), accounting for 97.54% of the spindle difference between K-complexes and SOs.
Conclusions: These findings highlight theta activity as a previously unrecognized mechanism linking cortical down-states to spindle dynamics, redefining the electrophysiological landscape of non-REM mechanisms supporting memory consolidation.
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