Abstract
AbstractNocturnal human sleep consists of 4 – 6 ninety-minute cycles defined as episodes of non-rapid eye movement (non-REM) sleep followed by an episode of REM sleep. While sleep cycles are considered fundamental components of sleep, their functional significance largely remains unclear. One of the reasons for a lack of research progress in this field is the absence of a “data-driven” definition of sleep cycles. Here, we proposed to base such a definition on fractal (aperiodic) neural activity, a well-established marker of arousal and sleep stages.We explored temporal dynamics of fractal activity during nocturnal sleep using electroencephalography. Based on the observed pattern of fractal fluctuations, we introduced a new concept, the “fractal” cycle of sleep, defined as a time interval during which fractal activity descends from its local maximum to its local minimum and then leads back to the next local maximum. Next, we assessed correlations between “fractal” and “classical” (i.e., non-REM – REM) sleep cycle durations. We also studied cycles with skipped REM sleep, i.e., the cycles where the REM phase is expected to appear except that it does not, being replaced by “lightening” of sleep.Regarding the sample, we examined fractal cycles in healthy adults (age range: 18 – 75 years, n = 205) as well as in children and adolescents (range: 8 – 17 years, n = 21), the group characterized by deeper sleep and a higher frequency of cycles with skipped REM sleep. Further, we studied “fractal” cycles in major depressive disorder (n = 111), the condition characterized by altered REM sleep (in addition to its clinical symptoms).We found that “fractal” and “classical” cycle durations (89 ± 34 min vs 90 ± 25 min) correlated positively (r = 0.5, p < 0.001). Cycle-to-cycle overnight dynamics showed an inverted U-shape of both fractal and classical cycle durations and a gradual decrease in absolute amplitudes of the fractal descents and ascents from early to late cycles.In adults, the “fractal” cycle duration and participant’s age correlated negatively (r = −0.2, p = 0.006). Children and adolescents had shorter “fractal” cycles compared to young adults (76 ± 34 vs 94 ± 32 min, p < 0.001). The fractal cycle algorithm detected cycles with skipped REM sleep in 53/55 (96%) cases.Medicated patients with depression showed longer “fractal” cycles compared to their own unmedicated state (107 ± 51 min vs 92 ± 38 min, p < 0.001) and age-matched controls (104 ± 49 vs 88 ± 31 min, p < 0.001).In conclusion, “fractal” cycles are an objective, quantifiable, continuous and biologically plausible way to display sleep neural activity and its cycles. They are useful in healthy adult and pediatric populations as well as in patients with major depressive disorder. “Fractal” cycles should be extensively studied to advance theoretical research on sleep structure.Highlights-The fractal sleep cycle is a new concept based on cyclic changes in fractal (aperiodic) neural activity during sleep.-Durations of fractal and classical cycles correlate, and both show an inverted U-shape when seen from early to late cycles.-The fractal cycle algorithm is effective in detecting cycles with skipped REM sleep.-Older healthy adults shower shorter “fractal” cycle durations.-Fractal cycle duration is shorter in children and adolescents compared to young adults.-In major depressive disorder, antidepressant medication is associated with longer fractal cycles.
Publisher
Cold Spring Harbor Laboratory