Fractal cycles of sleep: a new aperiodic activity-based definition of sleep cycles
eLife 13:RP96784, 2024
https://doi.org/10.7554/eLife.96784.1
Yevgenia Rosenblum1, Mahdad Jafarzadeh Esfahani1, Nico Adelhöfer1, Paul Zerr1, Melanie Furrer2, Reto Huber2,3, Axel Steiger4, Marcel Zeising5, Csenge G. Horváth6, Bence Schneider6, Róbert Bódizs6, Martin Dresler1
- Radboud University Medical Centre, Donders Institute for Brain, Cognition and Behavior, Nijmegen, Netherlands
- Child Development Center and Children’s Research Center, University Children’s Hospital Zürich, University of Zürich, Zürich, Switzerland
- Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric University Hospital Zurich, Zurich, Switzerland
- Max Planck Institute of Psychiatry, Munich, Germany
- Klinikum Ingolstadt, Centre of Mental Health, Ingolstadt, Germany
- Semmelweis University, Institute of Behavioural Sciences, Budapest, Hungary
ABSTRACT
Nocturnal 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 in 205 healthy adults aged 18 – 75 years. 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. Then, 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 replaced by “lightening” of sleep. Finally, we validated the fractal cycle concept 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, as well as in major depressive disorder (n = 111), the condition characterized by altered sleep structure (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 cycling nature. They are useful in healthy, pediatric and clinical populations and should be extensively studied to advance theoretical research on sleep structure.