Fundamentals of sleep regulation: Model and benchmark values for fractal and oscillatory neurodynamics
Homeostatic, circadian and ultradian mechanisms play crucial roles in the regulation of sleep. Evidence suggests that ratios of low-to-high frequency power in the electroencephalogram (EEG) spectrum indicate the instantaneous level of sleep pressure, influenced by factors such as individual sleep-wa...
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| Vydáno v: | Progress in neurobiology Ročník 234; s. 102589 |
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| Médium: | Journal Article |
| Jazyk: | angličtina |
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Elsevier Ltd
01.03.2024
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| ISSN: | 0301-0082, 1873-5118, 1873-5118 |
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| Abstract | Homeostatic, circadian and ultradian mechanisms play crucial roles in the regulation of sleep. Evidence suggests that ratios of low-to-high frequency power in the electroencephalogram (EEG) spectrum indicate the instantaneous level of sleep pressure, influenced by factors such as individual sleep-wake history, current sleep stage, age-related differences and brain topography characteristics. These effects are well captured and reflected in the spectral exponent, a composite measure of the constant low-to-high frequency ratio in the periodogram, which is scale-free and exhibits lower interindividual variability compared to slow wave activity, potentially serving as a suitable standardization and reference measure. Here we propose an index of sleep homeostasis based on the spectral exponent, reflecting the level of membrane hyperpolarization and/or network bistability in the central nervous system in humans. In addition, we advance the idea that the U-shaped overnight deceleration of oscillatory slow and fast sleep spindle frequencies marks the biological night, providing somnologists with an EEG-index of circadian sleep regulation. Evidence supporting this assertion comes from studies based on sleep replacement, forced desynchrony protocols and high-resolution analyses of sleep spindles. Finally, ultradian sleep regulatory mechanisms are indicated by the recurrent, abrupt shifts in dominant oscillatory frequencies, with spindle ranges signifying non-rapid eye movement and non-spindle oscillations – rapid eye movement phases of the sleep cycles. Reconsidering the indicators of fundamental sleep regulatory processes in the framework of the new Fractal and Oscillatory Adjustment Model (FOAM) offers an appealing opportunity to bridge the gap between the two-process model of sleep regulation and clinical somnology.
•Higher EEG frequency implies lower involvement in sleep homeostasis.•The sleep EEG spectral exponent depicts sleep homeostasis.•Oscillatory sleep spindle frequency indicates circadian regulation.•Spindle/non-spindle oscillation sequences follow ultradian rhythmicity.•Sleep regulatory processes are reframed in terms of fractal/oscillatory spectra. |
|---|---|
| AbstractList | Homeostatic, circadian and ultradian mechanisms play crucial roles in the regulation of sleep. Evidence suggests that ratios of low-to-high frequency power in the electroencephalogram (EEG) spectrum indicate the instantaneous level of sleep pressure, influenced by factors such as individual sleep-wake history, current sleep stage, age-related differences and brain topography characteristics. These effects are well captured and reflected in the spectral exponent, a composite measure of the constant low-to-high frequency ratio in the periodogram, which is scale-free and exhibits lower interindividual variability compared to slow wave activity, potentially serving as a suitable standardization and reference measure. Here we propose an index of sleep homeostasis based on the spectral exponent, reflecting the level of membrane hyperpolarization and/or network bistability in the central nervous system in humans. In addition, we advance the idea that the U-shaped overnight deceleration of oscillatory slow and fast sleep spindle frequencies marks the biological night, providing somnologists with an EEG-index of circadian sleep regulation. Evidence supporting this assertion comes from studies based on sleep replacement, forced desynchrony protocols and high-resolution analyses of sleep spindles. Finally, ultradian sleep regulatory mechanisms are indicated by the recurrent, abrupt shifts in dominant oscillatory frequencies, with spindle ranges signifying non-rapid eye movement and non-spindle oscillations - rapid eye movement phases of the sleep cycles. Reconsidering the indicators of fundamental sleep regulatory processes in the framework of the new Fractal and Oscillatory Adjustment Model (FOAM) offers an appealing opportunity to bridge the gap between the two-process model of sleep regulation and clinical somnology.Homeostatic, circadian and ultradian mechanisms play crucial roles in the regulation of sleep. Evidence suggests that ratios of low-to-high frequency power in the electroencephalogram (EEG) spectrum indicate the instantaneous level of sleep pressure, influenced by factors such as individual sleep-wake history, current sleep stage, age-related differences and brain topography characteristics. These effects are well captured and reflected in the spectral exponent, a composite measure of the constant low-to-high frequency ratio in the periodogram, which is scale-free and exhibits lower interindividual variability compared to slow wave activity, potentially serving as a suitable standardization and reference measure. Here we propose an index of sleep homeostasis based on the spectral exponent, reflecting the level of membrane hyperpolarization and/or network bistability in the central nervous system in humans. In addition, we advance the idea that the U-shaped overnight deceleration of oscillatory slow and fast sleep spindle frequencies marks the biological night, providing somnologists with an EEG-index of circadian sleep regulation. Evidence supporting this assertion comes from studies based on sleep replacement, forced desynchrony protocols and high-resolution analyses of sleep spindles. Finally, ultradian sleep regulatory mechanisms are indicated by the recurrent, abrupt shifts in dominant oscillatory frequencies, with spindle ranges signifying non-rapid eye movement and non-spindle oscillations - rapid eye movement phases of the sleep cycles. Reconsidering the indicators of fundamental sleep regulatory processes in the framework of the new Fractal and Oscillatory Adjustment Model (FOAM) offers an appealing opportunity to bridge the gap between the two-process model of sleep regulation and clinical somnology. Homeostatic, circadian and ultradian mechanisms play crucial roles in the regulation of sleep. Evidence suggests that ratios of low-to-high frequency power in the electroencephalogram (EEG) spectrum indicate the instantaneous level of sleep pressure, influenced by factors such as individual sleep-wake history, current sleep stage, age-related differences and brain topography characteristics. These effects are well captured and reflected in the spectral exponent, a composite measure of the constant low-to-high frequency ratio in the periodogram, which is scale-free and exhibits lower interindividual variability compared to slow wave activity, potentially serving as a suitable standardization and reference measure. Here we propose an index of sleep homeostasis based on the spectral exponent, reflecting the level of membrane hyperpolarization and/or network bistability in the central nervous system in humans. In addition, we advance the idea that the U-shaped overnight deceleration of oscillatory slow and fast sleep spindle frequencies marks the biological night, providing somnologists with an EEG-index of circadian sleep regulation. Evidence supporting this assertion comes from studies based on sleep replacement, forced desynchrony protocols and high-resolution analyses of sleep spindles. Finally, ultradian sleep regulatory mechanisms are indicated by the recurrent, abrupt shifts in dominant oscillatory frequencies, with spindle ranges signifying non-rapid eye movement and non-spindle oscillations - rapid eye movement phases of the sleep cycles. Reconsidering the indicators of fundamental sleep regulatory processes in the framework of the new Fractal and Oscillatory Adjustment Model (FOAM) offers an appealing opportunity to bridge the gap between the two-process model of sleep regulation and clinical somnology. Homeostatic, circadian and ultradian mechanisms play crucial roles in the regulation of sleep. Evidence suggests that ratios of low-to-high frequency power in the electroencephalogram (EEG) spectrum indicate the instantaneous level of sleep pressure, influenced by factors such as individual sleep-wake history, current sleep stage, age-related differences and brain topography characteristics. These effects are well captured and reflected in the spectral exponent, a composite measure of the constant low-to-high frequency ratio in the periodogram, which is scale-free and exhibits lower interindividual variability compared to slow wave activity, potentially serving as a suitable standardization and reference measure. Here we propose an index of sleep homeostasis based on the spectral exponent, reflecting the level of membrane hyperpolarization and/or network bistability in the central nervous system in humans. In addition, we advance the idea that the U-shaped overnight deceleration of oscillatory slow and fast sleep spindle frequencies marks the biological night, providing somnologists with an EEG-index of circadian sleep regulation. Evidence supporting this assertion comes from studies based on sleep replacement, forced desynchrony protocols and high-resolution analyses of sleep spindles. Finally, ultradian sleep regulatory mechanisms are indicated by the recurrent, abrupt shifts in dominant oscillatory frequencies, with spindle ranges signifying non-rapid eye movement and non-spindle oscillations – rapid eye movement phases of the sleep cycles. Reconsidering the indicators of fundamental sleep regulatory processes in the framework of the new Fractal and Oscillatory Adjustment Model (FOAM) offers an appealing opportunity to bridge the gap between the two-process model of sleep regulation and clinical somnology. •Higher EEG frequency implies lower involvement in sleep homeostasis.•The sleep EEG spectral exponent depicts sleep homeostasis.•Oscillatory sleep spindle frequency indicates circadian regulation.•Spindle/non-spindle oscillation sequences follow ultradian rhythmicity.•Sleep regulatory processes are reframed in terms of fractal/oscillatory spectra. |
| ArticleNumber | 102589 |
| Author | Horváth, Csenge G. Bódizs, Róbert Dresler, Martin Rosenblum, Yevgenia Schneider, Bence Ujma, Péter P. |
| Author_xml | – sequence: 1 givenname: Róbert surname: Bódizs fullname: Bódizs, Róbert email: bodizs.robert@med.semmelweis-univ.hu organization: Institute of Behavioural Sciences, Semmelweis University, Budapest, Hungary – sequence: 2 givenname: Bence surname: Schneider fullname: Schneider, Bence organization: Institute of Behavioural Sciences, Semmelweis University, Budapest, Hungary – sequence: 3 givenname: Péter P. surname: Ujma fullname: Ujma, Péter P. organization: Institute of Behavioural Sciences, Semmelweis University, Budapest, Hungary – sequence: 4 givenname: Csenge G. surname: Horváth fullname: Horváth, Csenge G. organization: Institute of Behavioural Sciences, Semmelweis University, Budapest, Hungary – sequence: 5 givenname: Martin surname: Dresler fullname: Dresler, Martin organization: Radboud University Medical Centre, Donders Institute for Brain, Cognition and Behavior, Nijmegen, the Netherlands – sequence: 6 givenname: Yevgenia surname: Rosenblum fullname: Rosenblum, Yevgenia organization: Radboud University Medical Centre, Donders Institute for Brain, Cognition and Behavior, Nijmegen, the Netherlands |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38458483$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_7554_eLife_96784_4 crossref_primary_10_1111_jsr_14439 crossref_primary_10_1002_acn3_70055 crossref_primary_10_1016_j_sleh_2025_01_007 crossref_primary_10_7554_eLife_96784 crossref_primary_10_1038_s41467_025_57766_x crossref_primary_10_1016_j_biopsych_2025_07_023 crossref_primary_10_1016_j_bbi_2025_05_002 |
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| Keywords | Fractional Brownian Motion Aperiodic Activity Fourier Analysis FOAM Sleep Stages Ultradian Rhythm Circadian Rhythm Polysomnography Neural Oscillations Historical Notes Sleep Homeostasis |
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