Fragments of wake-like activity frame down-states of sleep slow oscillations in humans: New vistas for studying homeostatic processes during sleep

During NREM sleep cortical activity corresponding to EEG fast rhythms (FRs >10 Hz) is interrupted by fragments of neural stillness (down-states), responsible for the negative peak within sleep slow oscillation (SSO). Researchers still debate whether the down-states spontaneously occur or need an initial overshoot in fluctuating activity. Herein, we studied temporally-isolated SSO in healthy subjects in order to identify two distinct EEG markers defining a putative initial up-state: i) a significant positive deflection and ii) an associated FR increase, before the negative peak. We found a positive bump preceding the down-state, which is detectable already at the cortical SSO origin site, both during N2 and N3. This early positive deflection, concurrent with a broadband activation, is characterized by an increase of sigma activity (12-18 Hz) from N2 to N3, while an opposite trend was observed for sigma activity crowning the up-state following the negative peak. Also, we found: (i) FR activations during up-states up to high gamma frequencies; (ii) depressed sigma activity in after-spindle recovery phase; and (iii) tightly coordinated activities between distinct bands (12-36 Hz, similar to 70 Hz, similar to 85 Hz and 105-125 Hz). The correlation between different bands suggested a common mechanism for sigma and gamma, and the pre-down-state activation associated with the initial bump suggested an activity ignition for down-state, whose intensity is dependent on sleep stage. In conclusion, we hypothesize that FR accompanying SSO could mark i) sleep homeostatic processes, such as the regulation/stabilization of sleep, counterbalancing the detrimental effects of continuous inputs from peripheries, and ii) neural mechanisms favoring the storage of information acquired during wakefulness. (C) 2013 Elsevier B.V. All rights reserved.