Grouping of Spindle Activity during Slow Oscillations in Human Non-Rapid Eye Movement Sleep

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Abstract
Based on findings primarily in cats, the grouping of spindle activity and fast brain oscillations by slow oscillations during slow-wave sleep (SWS) has been proposed to represent an essential feature in the processing of memories during sleep. We examined whether a comparable grouping of spindle and fast activity coinciding with slow oscillations can be found in human SWS. For negative and positive half-waves of slow oscillations (dominant frequency, 0.7–0.8 Hz) identified during SWS in humans (n = 13), wave-triggered averages of root mean square (rms) activity in the theta (4–8 Hz), alpha (8–12 Hz), spindle (12–15 Hz), and beta (15–25 Hz) range were formed. Slow positive half-waves were linked to a pronounced and widespread increase in rms spindle activity, averaging 0.63 ± 0.065 μV (23.4%; p < 0.001, with reference to baseline) at the midline central electrode (Cz). In contrast, spindle activity was suppressed during slow negative half-waves, on average by −0.65 ± 0.06 μV at Cz (−22%;p < 0.001). An increase in spindle activity 400–500 msec after negative half-waves was more than twofold the increase during slow positive half-waves (p< 0.001). A similar although less pronounced dynamic was observed for beta activity, but not for alpha and theta frequencies. Discrete spindles identified during stages 2 and 3 of non-rapid eye movement (REM) sleep coincided with a discrete slow positive half-wave-like potential preceded by a pronounced negative half-wave (p < 0.01). These results provide the first evidence in humans of grouping of spindle and beta activity during slow oscillations. They support the concept that phases of cortical depolarization during slow oscillations, reflected by surface-positive (depth-negative) field potentials, drive the thalamocortical spindle activity. The drive is particularly strong during cortical depolarization, expressed as surface-positive field potentials.