A new set of composite, non-redundant electroencephalogram measures of non-rapid eye movement sleep based on the power law scaling of the Fourier spectrum

AbstractA novel method for deriving composite, non-redundant measures of non-rapid eye movement (NREM) sleep electroencephalogram (EEG) is developed on the basis of the power law scaling of the Fourier spectra. Measures derived are the spectral intercept, the slope (spectral exponent), as well as the maximal whitened spectral peak amplitude and frequency in the sleep spindle range. As a proof of concept, we apply these measures on a large sleep EEG dataset (N = 175; 81 females; age range: 17–60 years) with previously demonstrated effects of age, sex and intelligence. As predicted, aging is associated with decreased overall spectral slopes (increased exponents) and whitened spectral peak amplitudes in the spindle frequency range. In addition, age associates with decreased sleep spindle spectral peak frequencies in the frontal region. Women were characterized by higher spectral intercepts and higher spectral peak frequencies in the sleep spindle range. No sex differences in whitened spectral peak amplitudes of the sleep spindle range were found. Intelligence correlated positively with whitened spectral peak amplitudes of the spindle frequency range in women, but not in men. Last, age-related increases in spectral exponents did not differ in subjects with average and high intelligence. Our findings replicate and complete previous reports in the literature, indicating that the number of variables describing NREM sleep EEG can be effectively reduced in order to overcome redundancy and Type I statistical errors in future electrophysiological studies of sleep.Author summaryGiven the tight reciprocal relationship between sleep and wakefulness, the objective description of the complex neural activity patterns characterizing human sleep is of utmost importance in understanding the several facets of brain function, like sex differences, aging and cognitive abilities. Current approaches are either exclusively based on visual impressions expressed in graded levels of sleep depth (W, N1, N2, N3, REM), whereas computerized quantitative methods provide an almost infinite number of potential metrics, suffering from significant redundancy and arbitrariness. Our current approach relies on the assumptions that the spontaneous human brain activity as reflected by the scalp-derived electroencephalogram (EEG) are characterized by coloured noise-like properties. That is, the contribution of different frequencies to the power spectrum of the signal are best described by power law functions with negative exponents. In addition, we assume, that stages N2–N3 are further characterized by additional non-random (non-noise like, sinusoidal) activity patterns, which are emerging at specific frequencies, called sleep spindles (9–18 Hz). By relying on these assumptions we were able to effectively reduce 191 spectral measures to 4: (1) the spectral intercept reflecting the overall amplitude of the signal, (2) the spectral slope reflecting the constant ratio of low over high frequency power, (3) the frequency of the maximal sleep spindle activity and (4) the amplitude of the sleep spindle spectral peak. These 4 measures were efficient in characterizing known age-effects, sex-differences and cognitive correlates of sleep EEG. Future clinical and basic studies are supposed to be significantly empowered by the efficient data reduction provided by our approach.

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A set of composite, non-redundant EEG measures of NREM sleep based on the power law scaling of the Fourier spectrum

Scientific Reports ◽

10.1038/s41598-021-81230-7 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Róbert Bódizs ◽

Orsolya Szalárdy ◽

Csenge Horváth ◽

Péter P. Ujma ◽

Ferenc Gombos ◽

...

Keyword(s):

Sex Differences ◽

Power Law ◽

Cognitive Abilities ◽

Brain Activity ◽

Nrem Sleep ◽

Scale Free ◽

Cognitive Correlates ◽

Efficient Data ◽

Basic Studies ◽

Electroencephalogram Eeg

AbstractFeatures of sleep were shown to reflect aging, typical sex differences and cognitive abilities of humans. However, these measures are characterized by redundancy and arbitrariness. Our present approach relies on the assumptions that the spontaneous human brain activity as reflected by the scalp-derived electroencephalogram (EEG) during non-rapid eye movement (NREM) sleep is characterized by arrhythmic, scale-free properties and is based on the power law scaling of the Fourier spectra with the additional consideration of the rhythmic, oscillatory waves at specific frequencies, including sleep spindles. Measures derived are the spectral intercept and slope, as well as the maximal spectral peak amplitude and frequency in the sleep spindle range, effectively reducing 191 spectral measures to 4, which were efficient in characterizing known age-effects, sex-differences and cognitive correlates of sleep EEG. Future clinical and basic studies are supposed to be significantly empowered by the efficient data reduction provided by our approach.

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146 Better Aerobic Fitness Is Associated with Distinct Sleep Characteristics in Adolescents

SLEEP ◽

10.1093/sleep/zsab072.145 ◽

2021 ◽

Vol 44 (Supplement_2) ◽

pp. A60-A60

Author(s):

Ariel Neikrug ◽

Shlomit Radom-Aizik ◽

Ivy Chen ◽

Annamarie Stehli ◽

Kitty Lui ◽

...

Keyword(s):

Eye Movement ◽

Slow Wave ◽

Aerobic Fitness ◽

Nrem Sleep ◽

Brain Maturation ◽

Rapid Eye Movement ◽

Sleep Spindle ◽

Sleep Patterns ◽

Peak Vo2 ◽

Local Sleep

Abstract Introduction Aerobic fitness facilitates brain synaptic plasticity, which influences global and local sleep expression. While it is known that sleep patterns/behavior and non-rapid eye movement (NREM) sleep slow wave activity (SWA) tracks brain maturation, little is known about how aerobic fitness and sleep interact during development in youth. The aim of this pilot was to characterize relationships among aerobic fitness, measures of global/local sleep expression, and habitual sleep patterns in children and adolescents. We hypothesized that greater aerobic fitness would be associated with better sleep quality, indicated by increased SWA. Methods 20 adolescents (mean age=14.6±2.3 years old, range 11-17, 11 females) were evaluated for AF (peak VO2 assessed by ramp-type progressive cycle ergometry in the laboratory), habitual sleep duration and efficiency (continuous 7-14 day actigraphy with sleep diary), and topographic patterns of spectral power in slow wave, theta, and sleep spindle frequency ranges in non-rapid eye movement (NREM) sleep using overnight polysomnography with high-density electroencephalography (hdEEG, 128 channels). Results Significant relationships were observed between peak VO2 and habitual bedtime (r=-0.604, p=0.013) and wake-up time (r=-0.644, p=0.007), with greater fitness associated with an earlier sleep schedule (going to bed and waking up earlier). Peak VO2 was a significant predictor of slow oscillations (0.5-1Hz, p=0.018) and theta activity (4.5-7.5Hz, p=0.002) over anterior frontal and central derivations (p<0.001 and p=0.001, respectively) after adjusting for sex and pubertal development stage. Similar associations were detected for fast sleep spindle activity (13-16Hz, p=0.006), which was greater over temporo-parietal derivations. Conclusion Greater AF was associated with earlier habitual sleep times and with enhanced expression of developmentally-relevant sleep oscillations during NREM sleep. These data suggest that AF may 1) minimize the behavioral sleep delay commonly seen during adolescence, and 2) impact topographically-specific features of sleep physiology known to mechanistically support neuroplasticity and cognitive processes which are dependent on prefrontal cortex and hippocampal function in adolescents and adults. Support (if any) NCATS grant #UL1TR001414 & PERC Systems Biology Fund

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NREM delta stimulation following MK-801 is a response of sleep systems

Journal of Neurophysiology ◽

10.1152/jn.1996.76.6.3714 ◽

1996 ◽

Vol 76 (6) ◽

pp. 3714-3720 ◽

Cited By ~ 27

Author(s):

I. G. Campbell ◽

I. Feinberg

Keyword(s):

Sleep Deprivation ◽

Eye Movement ◽

Time Course ◽

Sleep Onset ◽

Nrem Sleep ◽

Rapid Eye Movement ◽

Mk 801 ◽

Regulatory Systems ◽

Sleep Centers ◽

Electroencephalogram Eeg

1. We have previously shown that noncompetitive blockade of the N-methyl-D-aspartate (NMDA)-gated cation channel with ketamine or Dizocilpine maleate (MK-801) increases the intensity of non-rapid-eye-movement (NREM) delta during subsequent sleep. This delta increase [measured as integrated amplitude (IA) in 1- to 4-Hz electroencephalogram (EEG)] occurs in the 12-h period following intraperitoneal injection. However, the 12 h after drug injection is also the period in which these drugs induce neurotoxic changes, raising the possibility that the increased delta represents toxic EEG slowing rather than an increase in the physiological delta waves of NREM sleep. 2. We hypothesized that the time course of delta stimulation could be separated from the time course of neurotoxicity. We tested this hypothesis by injecting 0.3 mg/kg MK-801 at the start of the dark period (DP) and depriving rats of sleep until the onset of the light period (LP) 12 h later. 3. There were two control groups: one received MK-801 at the start of the DP with no further manipulation, and the second received a saline injection at DP onset followed by 12 h of sleep deprivation. The dependent variable was the amount of delta IA in the LP, whose onset was 12 h after MK-801 injection. Total IA in the LP was significantly greater in rats that received MK-801 followed by sleep deprivation than in rats that received sleep deprivation alone or MK-801 alone. 4. This finding indicates that delta stimulation by MK-801 is maintained over 12 h of waking, indicating that the delta increase is not due to toxic EEG slowing or persisting MK-801. Instead, NMDA channel blockade by MK-801 increases the homeostatic need for delta or else directly alters sleep regulatory systems. We speculate that these effects are mediated by hypothalamic sleep centers through control of neuroendocrine pulses that produce both NREM and rapid-eye-movement sleep. 5. Imposing a period of waking between drug administration and sleep onset may prove a generally useful strategy for determining whether a drug affects the homeostatic need for sleep or acutely stimulates sleep systems. This strategy can also help distinguish between toxic and physiological increases in delta EEG.

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Spindles are highly heritable as identified by different spindle detectors

SLEEP ◽

10.1093/sleep/zsaa230 ◽

2020 ◽

Author(s):

Jennifer R Goldschmied ◽

Karine Lacourse ◽

Greg Maislin ◽

Jacques Delfrate ◽

Philip Gehrman ◽

...

Keyword(s):

Detection Method ◽

Sleep Spindles ◽

Sleep Spindle ◽

Frequency Range ◽

Same Sex ◽

Detection Algorithms ◽

Detector Method ◽

Scalp Location ◽

Electroencephalogram Eeg ◽

Robust Evidence

Abstract Study Objectives Sleep spindles, a defining feature of stage N2 sleep, are maximal at central electrodes and are found in the frequency range of the electroencephalogram (EEG) (sigma 11–16 Hz) that is known to be heritable. However, relatively little is known about the heritability of spindles. Two recent studies investigating the heritability of spindles reported moderate heritability, but with conflicting results depending on scalp location and spindle type. The present study aimed to definitively assess the heritability of sleep spindle characteristics. Methods We utilized the polysomnography data of 58 monozygotic and 40 dizygotic same-sex twin pairs to identify heritable characteristics of spindles at C3/C4 in stage N2 sleep including density, duration, peak-to-peak amplitude, and oscillation frequency. We implemented and tested a variety of spindle detection algorithms and used two complementary methods of estimating trait heritability. Results We found robust evidence to support strong heritability of spindles regardless of detector method (h2 > 0.8). However not all spindle characteristics were equally heritable, and each spindle detection method produced a different pattern of results. Conclusions The sleep spindle in stage N2 sleep is highly heritable, but the heritability differs for individual spindle characteristics and depends on the spindle detector used for analysis.

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Muscimol and Midazolam Do Not Potentiate Each Other's Effects on Sleep EEG in the Rat

Journal of Neurophysiology ◽

10.1152/jn.1997.77.3.1624 ◽

1997 ◽

Vol 77 (3) ◽

pp. 1624-1629 ◽

Cited By ~ 21

Author(s):

Marike Lancel ◽

Johannes Faulhaber ◽

Thomas Schiffelholz ◽

Stefan Mathias ◽

Rudolf A. Deisz

Keyword(s):

Random Order ◽

Sleep Eeg ◽

Rapid Eye Movement Sleep ◽

Frequency Range ◽

Light Onset ◽

Eeg Activity ◽

Combined Administration ◽

Sleep Parameters ◽

Induced Changes ◽

Electroencephalogram Eeg

Lancel, Marike, Johannes Faulhaber, Thomas Schiffelholz, Stefan Mathias, and Rudolf A. Deisz. Muscimol and midazolam do not potentiate each other's effects on sleep EEG in the rat. J. Neurophysiol. 77: 1624–1629, 1997. The interaction of a γ-aminobutyric acid-A (GABAA) receptor agonist and a benzodiazepine-type modulator of GABAA receptors on sleep was investigated. Low doses of muscimol (0.3 mg/kg) and the benzodiazepine midazolam (1.5 mg/kg) were administered alone and incombination, in random order, to eight rats. All injections were given intraperitoneally at light onset. Electroencephalogram (EEG) and electromyogram were recorded during the first 6 h post injection. Compared with vehicle, muscimol hardly affected the time spent in non-rapid eye movement sleep (non-REMS) and REMS, but significantly enhanced EEG activity in the frequency range between 2 and 6 Hz during non-REMS. Midazolam significantly increased the time spent in non-REMS, reduced EEG activity at frequencies <12 Hz, and elevated EEG activity in most higher frequencies during this state. The combined administration of muscimol and midazolam affected non-REMS-specific EEG activity in an unexpected fashion: the effects were intermediate between those of muscimol and midazolam. These results indicate that muscimol and midazolam have dissimilar effects on EEG within non-REMS and demonstrate that midazolam does not augment but attenuates the muscimol-induced changes in sleep EEG. Our data are at variance with established mechanisms, according to which agonistic modulators would have similar effects and should potentiate the effects of GABAA agonists. The present data suggest that application of agonists and agonistic modulators of GABAA receptors causes differential net effects on sleep parameters.

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Cellular Composition of the Preoptic Area Regulating Sleep, Parental, and Sexual Behavior

Frontiers in Neuroscience ◽

10.3389/fnins.2021.649159 ◽

2021 ◽

Vol 15 ◽

Author(s):

Yousuke Tsuneoka ◽

Hiromasa Funato

Keyword(s):

Eye Movement ◽

Preoptic Area ◽

Steroid Receptors ◽

Activity Patterns ◽

Nrem Sleep ◽

Sexually Dimorphic ◽

Rapid Eye Movement ◽

Reproductive Behaviors ◽

Innate Behaviors

The preoptic area (POA) has long been recognized as a sleep center, first proposed by von Economo. The POA, especially the medial POA (MPOA), is also involved in the regulation of various innate functions such as sexual and parental behaviors. Consistent with its many roles, the MPOA is composed of subregions that are identified by different gene and protein expressions. This review addresses the current understanding of the molecular and cellular architecture of POA neurons in relation to sleep and reproductive behavior. Optogenetic and pharmacogenetic studies have revealed a diverse group of neurons within the POA that exhibit different neural activity patterns depending on vigilance states and whose activity can enhance or suppress wake, non-rapid eye movement (NREM) sleep, or rapid eye movement (REM) sleep. These sleep-regulating neurons are not restricted to the ventrolateral POA (VLPO) region but are widespread in the lateral MPOA and LPOA as well. Neurons expressing galanin also express gonadal steroid receptors and regulate motivational aspects of reproductive behaviors. Moxd1, a novel marker of sexually dimorphic nuclei (SDN), visualizes the SDN of the POA (SDN-POA). The role of the POA in sleep and other innate behaviors has been addressed separately; more integrated observation will be necessary to obtain physiologically relevant insight that penetrates the different dimensions of animal behavior.

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A Motor Theory of Sleep-Wake Control: Arousal-Action Circuit

Annual Review of Neuroscience ◽

10.1146/annurev-neuro-080317-061813 ◽

2019 ◽

Vol 42 (1) ◽

pp. 27-46 ◽

Cited By ~ 28

Author(s):

Danqian Liu ◽

Yang Dan

Keyword(s):

Eye Movement ◽

Nrem Sleep ◽

Distributed Networks ◽

Rapid Eye Movement ◽

The Past ◽

Motor Circuits ◽

Intimate Association ◽

Control Circuits ◽

Function Of Sleep ◽

Electroencephalogram Eeg

Wakefulness, rapid eye movement (REM) sleep, and non–rapid eye movement (NREM) sleep are characterized by distinct electroencephalogram (EEG), electromyogram (EMG), and autonomic profiles. The circuit mechanism coordinating these changes during sleep-wake transitions remains poorly understood. The past few years have witnessed rapid progress in the identification of REM and NREM sleep neurons, which constitute highly distributed networks spanning the forebrain, midbrain, and hindbrain. Here we propose an arousal-action circuit for sleep-wake control in which wakefulness is supported by separate arousal and action neurons, while REM and NREM sleep neurons are part of the central somatic and autonomic motor circuits. This model is well supported by the currently known sleep and wake neurons. It can also account for the EEG, EMG, and autonomic profiles of wake, REM, and NREM states and several key features of their transitions. The intimate association between the sleep and autonomic/somatic motor control circuits suggests that a primary function of sleep is to suppress motor activity.

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Sex differences within sleep in gonadally intact rats

SLEEP ◽

10.1093/sleep/zsz289 ◽

2019 ◽

Vol 43 (5) ◽

Cited By ~ 6

Author(s):

Kevin M Swift ◽

Karina Keus ◽

Christy Gonzalez Echeverria ◽

Yesenia Cabrera ◽

Janelly Jimenez ◽

...

Keyword(s):

Sex Differences ◽

Estrous Cycle ◽

Eye Movement ◽

Rem Sleep ◽

Spectral Power ◽

Nrem Sleep ◽

Brain Regions ◽

Spectral Coherence ◽

Physiological Processes ◽

Neural Processes

Abstract Sleep impacts diverse physiological and neural processes and is itself affected by the menstrual cycle; however, few studies have examined the effects of the estrous cycle on sleep in rodents. Studies of disease mechanisms in females therefore lack critical information regarding estrous cycle influences on relevant sleep characteristics. We recorded electroencephalographic (EEG) activity from multiple brain regions to assess sleep states as well as sleep traits such as spectral power and interregional spectral coherence in freely cycling females across the estrous cycle and compared with males. Our findings show that the high hormone phase of proestrus decreases the amount of nonrapid eye movement (NREM) sleep and rapid eye movement (REM) sleep and increases the amount of time spent awake compared with other estrous phases and to males. This spontaneous sleep deprivation of proestrus was followed by a sleep rebound in estrus which increased NREM and REM sleep. In proestrus, spectral power increased in the delta (0.5–4 Hz) and the gamma (30–60 Hz) ranges during NREM sleep, and increased in the theta range (5–9 Hz) during REM sleep during both proestrus and estrus. Slow-wave activity (SWA) and cortical sleep spindle density also increased in NREM sleep during proestrus. Finally, interregional NREM and REM spectral coherence increased during proestrus. This work demonstrates that the estrous cycle affects more facets of sleep than previously thought and reveals both sex differences in features of the sleep–wake cycle related to estrous phase that likely impact the myriad physiological processes influenced by sleep.

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145 Aerobic Fitness Is Associated with Advanced Circadian Rhythms in Adolescents

SLEEP ◽

10.1093/sleep/zsab072.144 ◽

2021 ◽

Vol 44 (Supplement_2) ◽

pp. A59-A60

Author(s):

Ariel Neikrug ◽

Shlomit Radom-Aizik ◽

Ivy Chen ◽

Annamarie Stehli ◽

Kitty Lui ◽

...

Keyword(s):

Eye Movement ◽

Slow Wave ◽

Aerobic Fitness ◽

Nrem Sleep ◽

Brain Maturation ◽

Rapid Eye Movement ◽

Sleep Spindle ◽

Sleep Patterns ◽

Peak Vo2 ◽

Local Sleep

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Detrended Fluctuation Analysis Features for Automated Sleep Staging of Sleep EEG

International Journal of Systems Biology and Biomedical Technologies ◽

10.4018/ijsbbt.2012100104 ◽

2012 ◽

Vol 1 (4) ◽

pp. 47-59 ◽

Cited By ~ 1

Author(s):

Amr F. Farag ◽

Shereen M. El-Metwally

Keyword(s):

Eye Movement ◽

Power Law ◽

Detrended Fluctuation Analysis ◽

Sleep Eeg ◽

Sleep Stages ◽

Fluctuation Analysis ◽

Eeg Signal ◽

Rapid Eye Movement ◽

Sleep Staging ◽

Detrended Fluctuation

An accurate sleep staging is crucial for the treatment of sleep disorders. Recently some studies demonstrated that the long range correlations of many physiological signals measured during sleep show some variations during the different sleep stages. In this study, detrended fluctuation analysis (DFA) is used to study the electroencephalogram (EEG) signal autocorrelation during different sleep stages. A classification of these stages is then made by introducing the calculated DFA power law exponents to a K-Nearest Neighbor classifier. The authors’ study reveals that a 2-D feature space composed of the DFA power law exponents of both the filtered THETA and BETA brain waves resulted in a classification accuracy of 93.52%, 93.52%, and 92.59% for the wake, non-rapid eye movement and rapid eye movement stages, respectively. The overall accuracy of the proposed system is 93.21%. The authors conclude that it might be possible to build an automated sleep assessment system based on DFA analysis of the sleep EEG signal.

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