Spindle and slow wave rhythms at slow wave sleep transitions are linked to strong shifts in the cortical direct current potential

Electroencephalographic activity at the transition from wakefulness to sleep is characterized by the appearance of spindles (12-15 Hz) and slow wave rhythms including delta activity (1-4 Hz) and slow oscillations (0.2-1 Hz). While these rhythms originate within neocortico-thalamic circuitry, their emergence during the passage into slow wave sleep (SWS) critically depends on the activity of neuromodulatory systems. Here, we examined the temporal relationships between these electroencephalogram rhythms and the direct current (DC) potential recorded from the scalp in healthy men (n=10) using cross-correlation analyses. Analyses focused on transitions from wakefulness to SWS in the beginning of the sleep period, and from SWS to lighter sleep and rapid eye movement (REM) sleep at the end of the first sleep cycle. For spindle, delta and slow oscillatory activity strong negative correlations with the DC potential were found at the transition into SWS with peak correlation coefficients (at zero time lag) averaging r=-0.81, -0.88 and -0.88, respectively (P<0.001). Though slightly lower, distinct negative correlations between these measures were also found at the transition from SWS to REM sleep (-0.78, -0.77 and -0.77, respectively, P<0.001). Fast oscillatory activity in the beta frequency band (15-25 Hz) was correlated positively with the DC potential (r=+0.75, P<0.05, at the passage to SWS). Data indicate close links between increasing spindle, delta and slow oscillatory activity and the occurrence of a steep surface negative cortical DC potential shift during the transition from wake to SWS. Likewise, a DC potential shift toward surface positivity accompanies the disappearance of these oscillatory phenomena at the end of the non-REM sleep period. The DC potential shifts may reflect gradual changes in extracellular ionic (Ca ²⁺) concentration resulting from the generation of spindle and slow wave rhythms, or influences of neuromodulating systems on cortical excitability thereby controlling the emergence of cortical spindle and slow wave rhythms at SWS transitions.