Effect of prolonged wakefulness on electroencephalographic oscillatory activity during sleep

The human sleep electroencephalogram (EEG) is characterized by the occurrence of distinct oscillatory events such as delta waves, sleep spindles and alpha activity. We applied a previously proposed algorithm for the detection of such events and investigated their incidence and frequency in baseline and recovery sleep after 40 h of sustained wakefulness in 27 healthy young subjects. The changes in oscillatory events induced by sleep deprivation were compared to the corresponding spectral changes. Both approaches revealed, on average, an increase in low frequency activity and a decrease in spindle activity after sleep deprivation. However, the increase of oscillatory events in the delta range and decrease in the sigma range occurred in a more restricted frequency range compared to spectral changes. The mean relative power spectra showed a significant increase in theta and alpha activity after sleep deprivation while, on average, the event analysis showed only a weak effect in the theta band. The reason for this discrepancy is that the spectral analysis does not distinguish between diffuse activity and clearly visible temporally localized oscillations, while the event analysis would detect only the latter. Additionally, only a few individuals clearly showed activity in the theta or alpha frequency bands. Conversely, event analysis revealed that some individuals showed an increased rate of sleep spindles after sleep deprivation, a fact that was not evident in the relative power spectra due to a decrease in background activity. The two methods complement each other and facilitate the interpretation of distinct changes induced by prolonged wakefulness in sleep EEG.     

The effects of age and gender on sleep EEG power spectral density in the middle years of life (ages 20-60 years old)

The effects of age and gender on sleep EEG power spectral density were assessed in a group of 100 subjects aged 20 to 60 years. We propose a new statistical strategy (mixed-model using fixed-knot regression splines) to analyze quantitative EEG measures. The effect of gender varied according to frequency, but no interactions emerged between age and gender, suggesting that the aging process does not differentially influence men and women. Women had higher power density than men in delta, theta, low alpha, and high spindle frequency range. The effect of age varied according to frequency and across the night. The decrease in power with age was not restricted to slow-wave activity, but also included theta and sigma activity. With increasing age, the attenuation over the night in power density between 1.25 and 8.00 Hz diminished, and the rise in power between 12.25 and 14.00 Hz across the night decreased. Increasing age was associated with higher power in the beta range. These results suggest that increasing age may be related to an attenuation of homeostatic sleep pressure and to an increase in cortical activation during sleep.     

Age effects on spectral electroencephalogram activity prior to dream recall

Ageing is associated with marked changes in sleep timing, structure and electroencephalographic (EEG) activity. Older people exhibit less slow-wave and spindle activity during non-rapid eye movement (NREM) sleep, together with attenuated levels of rapid eye movement (REM) sleep as compared to young individuals. However, the extent to which these age-related changes in sleep impact on dream processing remains largely unknown. Here we investigated NREM and REM sleep EEG activity prior to dream recall and no recall in 17 young (20-31 years) and 15 older volunteers (57-74 years) during a 40 h multiple nap protocol. Dream recall was assessed immediately after each nap. During NREM sleep prior to dream recall, older participants displayed higher frontal EEG delta activity (1-3 Hz) and higher centro-parietal sigma activity (12-15 Hz) than the young volunteers. Conversely, before no recall, older participants had less frontal-central delta activity and less sigma activity in frontal, central and parietal derivations than the young participants. REM sleep was associated to age-related changes, such that older participants had less frontal-central alpha (10-12 Hz) and beta (16-19 Hz) activity, irrespective of dream recall and no recall. Our data indicate that age-related differences in dream recall seem to be directly coupled to specific frequency and topography EEG patterns, particularly during NREM sleep. Thus, the spectral correlates of dreaming can help to understand the cortical pathways of dreaming.     

A comparison of period amplitude analysis and FFT power spectral analysis of all-night human sleep EEG.

Zero-cross and zero-derivative period amplitude analysis (PAA) data were compared with power spectral analysis (PSA) data obtained with the fast Fourier transform in all-night sleep EEG from 10 subjects. Although PAA zero-cross-integrated amplitude showed good agreement with PSA power in 0.3-2 Hz, zero-cross analysis appears relatively ineffective in measuring 2-4 Hz and above waves. However, PAA zero-derivative measures of peak-trough amplitude correlated well with PSA power in 2-4 Hz. Thus, while PAA appears able to measure the entire EEG spectrum, the analytic technique should be changed from zero cross to zero derivative at about 2 Hz in human sleep EEG. PAA and PSA both demonstrate robust and interrelated across-night oscillations in three frequency bands: delta (0.3-4 Hz); sigma (12-16 Hz); and fast beta (20-10 Hz). The frequencies between delta and sigma, and between sigma and fast beta, did not show clear across-night oscillations using either method, and the two methods showed lower epoch-to-epoch agreement in these intermediate bands. The causes of this reduced agreement are not immediately clear, nor is it obvious which method gives more valid results. We believe that the three strongly oscillating frequency bands represent fundamental properties of the human sleep EEG that provide important clues to underlying physiological mechanisms. These mechanisms are more likely to be understood if their dynamic properties are preserved and measured naturalistically rather than being forced into arbitrary sleep stages or procrustean models. Both PAA and PSA can be employed for such naturalistic studies. PSA has the advantages of applying the same analytic method across the EEG spectrum and rests on more fully developed theory. Combined zero-cross and zero-derivative PAA demonstrates EEG oscillations that closely parallel those observed with spectral power, and the PAA measures do not rely on assumptions about the spectral composition of the signal. In addition, both PAA techniques can measure the relative contributions of wave amplitude and incidence to total power: These waveform characteristics represent different biological processes and respond differentially to a wide range of experimental conditions.     

Dynamic changes in electroencephalogram spectral power with varying apnea duration in older adults

Sleep apnea elicits brain and physiological changes and its duration varies across the night. This study investigates the changes in the relative powers in electroencephalogram (EEG) frequency bands before and at apnea termination and as a function of apnea duration. The analysis was performed on 30 sleep records (375 apnea events) of older adults diagnosed with sleep apnea. Power spectral analysis centered on two 10‐s EEG epochs, before apnea termination (BAT) and after apnea termination (AAT), for each apnea event. The relative power changes in EEG frequency bands were compared with changes in apnea duration, defined as Short (between 10 and 20 s), Moderate (between 20 and 30 s) and Long (between 30 and 40 s). A significant reduction in EEG relative powers for lower frequency bands of alpha and sigma were observed for the Long compared to the Moderate and Short apnea duration groups at BAT, and reduction in relative theta, alpha and sigma powers for the Long compared to the Moderate and Short groups at AAT. The proportion of apnea events showed a significantly decreased trend with increased apnea duration for non‐rapid eye movement sleep but not rapid eye movement sleep. The proportion of central apnea events decreased with increased apnea duration, but not obstructive episodes. The findings suggest EEG arousal occurred both before and at apnea termination and these transient arousals were associated with a reduction in relative EEG powers of the low‐frequency bands: theta, alpha and sigma. The clinical implication is that these transient EEG arousals, without awakenings, are protective of sleep. Further studies with large datasets and different age groups are recommended.     

Heartbeat‐related EEG amplitude and phase modulations from wakefulness to deep sleep: Interactions with sleep spindles and slow oscillations

Based on physiological models of neurovisceral integration, different studies have shown how cognitive processes modulate heart rate and how the heartbeat, on the other hand, modulates brain activity. We tried to further determine interactions between cardiac and electrical brain activity by means of EEG. We investigated how the heartbeat modulates EEG in 23 healthy controls from wakefulness to deep sleep and showed that frontocentral heartbeat evoked EEG amplitude and phase locking (as measured by intertrial phase locking), at about 300‐400 ms after the R peak, decreased with increasing sleep depth with a renewed increase during REM sleep, which underpins the assumption that the heartbeat evoked positivity constitutes an active frontocortical response to the heartbeat. Additionally, we found that individual heart rate was correlated with the frequency of the EEG's spectral peak (i.e., alpha peak frequency during wakefulness). This correlation was strongest during wakefulness and declined linearly with increasing sleep depth. Furthermore, we show that the QRS complex modulates spindle phase possibly related to the correspondence between the frequency of the QRS complex and the spindle frequency of about 12–15 Hz. Finally, during deep sleep stages, a loose temporal coupling between heartbeats and slow oscillation (0.8 Hz) could be observed. These findings indicate that cardiac activity such as heart rate or individual heartbeats can modulate or be modulated by ongoing oscillatory brain activity.     

Separation of circadian and wake duration-dependent modulation of EEG activation during wakefulness

The separate contribution of circadian rhythmicity and elapsed time awake on electroencephalographic (EEG) activity during wakefulness was assessed. Seven men lived in an environmental scheduling facility for 4 weeks and completed fourteen 42.85-h 'days', each consisting of an extended (28.57-h) wake episode and a 14.28-h sleep opportunity. The circadian rhythm of plasma melatonin desynchronized from the 42.85-h day. This allowed quantification of the separate contribution of circadian phase and elapsed time awake to variation in EEG power spectra (1-32 Hz). EEG activity during standardized behavioral conditions was markedly affected by both circadian phase and elapsed time awake in an EEG frequency- and derivation-specific manner. The nadir of the circadian rhythm in alpha (8-12 Hz) activity in both fronto-central and occipito-parietal derivations occurred during the biological night, close to the crest of the melatonin rhythm. The nadir of the circadian rhythm of theta (4.5-8 Hz) and beta (20-32 Hz) activity in the fronto-central derivation was located close to the onset of melatonin secretion, i.e. during the wake maintenance zone. As time awake progressed, delta frequency (1-4.5 Hz) and beta (20-32 Hz) activity rose monotonically in frontal derivations. The interaction between the circadian and wake-dependent increase in frontal delta was such that the intrusion of delta was minimal when sustained wakefulness coincided with the biological day, but pronounced during the biological night. Our data imply that the circadian pacemaker facilitates frontal EEG activation during the wake maintenance zone, by generating an arousal signal that prevents the intrusion of low-frequency EEG components, the propensity for which increases progressively during wakefulness.     

Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans

SUMMARY  The hypothesis that local activation of brain regions during wakefulness affects the EEG recorded from these regions during sleep was tested by applying vibratory stimuli to one hand prior to sleep. Eight subjects slept in the laboratory for five consecutive nights. During a 6-h period prior to night 3, either the left or the right hand was vibrated intermittently (20 min on-8 min off), while prior to night 5 the same treatment was applied to the contralateral hand. The sleep EEG was recorded from frontal, central, parietal and occipital derivations and subjected to spectral analysis. The interhemispheric asymmetry index (IAI) was calculated for spectral power in nonREM sleep in the frequency range 0.25-25.0 Hz for 0.5-Hz or 1-Hz bins. In the first hour of sleep following right-hand stimulation, the IAI of the central derivation was increased relative to baseline, which corresponds to a shift of power towards the left hemisphere. This effect was most prominent in the delta range, was limited to the first hour of sleep and was restricted to the central derivation situated over the somatosensory cortex. No significant changes were observed following left-hand stimulation. Although the effect was small, it is consistent with the hypothesis that the activation of specific neuronal populations during wakefulness may have repercussions on their electrical activity pattern during subsequent sleep.     

Homeostatic behavior of fast Fourier transform power in very low frequency non-rapid eye movement human electroencephalogram

Basic research shows that the physiological and molecular mechanisms of very low frequency (<1 Hz) electroencephalogram (EEG) waves of non-rapid eye movement (NREM) sleep differ from those of the higher (1–4 Hz) delta frequencies. Human studies show that the across-NREM period dynamics of very low frequency and 1–4 Hz EEG also differ. These differences and the reported failure of very low frequency EEG power to increase after a night of total sleep deprivation raise the question of whether very low frequency EEG shows the other homeostatic properties established for higher delta frequencies. Here we tested the relation of very low frequency EEG power density to prior waking duration across a normal day and whether these low frequencies meet another criterion for homeostatic sleep EEG: conservation of power across a late nap and post-nap sleep. Data from 19 young adults recorded in four separate sessions of baseline, daytime nap and post-nap sleep were analyzed. Power density in very low frequency NREM EEG increased linearly when naps were taken later in the day (i.e. were preceded by longer waking durations). In the night following an 18:00 h nap, very low frequency power was reduced by roughly the amount of power in the nap. Thus, very low frequency EEG meets two major homeostatic criteria. We hypothesize that these low frequencies reflect the executive rather than the functional processes by which NREM sleep reverses the effects of waking brain activity.     

EEG spectral power analysis of phasic and tonic REM sleep in young and older male subjects

EEG spectral power was studied during periods of rapid eye movements (REMs) and tonic intervals in REM sleep of 7 young and 7 older male subjects. Significant symmetrical decreases in alpha and beta1 power at central and occipital sites, concurrent with an increase in frontal theta power, were observed during the production of REMs. The former findings are discussed as sleep analogues to changes in alpha and beta1 during waking, showing increased information processing and behavioural activation, and that of theta is tentatively presented as reflecting an increase in afferent thresholds. Independent of the phasic-tonic REM distinction, total EEG power markedly decreased as a function of time of night and did not interact with age. Significant age differences in the overall spectral composition of the EEG were obtained, namely, a lower level of delta power and a relative shift towards more power in frequencies above 12 Hz for the older group. Further, older subjects also demonstrated a more uniform topographical distribution of alpha and sigma power.     

Regional differences of the sleep electroencephalogram in adolescents

The sleep electroencephalogram (EEG) was recorded from anterior (Fz/Cz) and posterior (Pz/Oz) bipolar derivations in two developmental groups: 20 pre- or early pubertal (Tanner 1/2, mean age 11.4 +/- 1.1 years, 11 boys) and 20 late pubertal or mature adolescents (Tanner 4/5, 14.1 +/- 1.3 years, 8 boys). A sleep-state independent reduction of EEG power over almost the entire frequency range was present in Tanner 4/5 compared with Tanner 1/2 adolescents. Spectral characteristics of the sleep EEG yielded state- and frequency-dependent regional differences that were similar in both developmental groups. Anterior predominance of power in delta and sigma ranges occurred in non-rapid eye movement sleep. Rapid eye movement sleep EEG power was greater in low delta, alpha, and sigma ranges for the posterior derivation and in theta and beta ranges for the anterior derivation. The decay rate of the sleep homeostatic process--reflected by the exponential decline of the 2-Hz EEG power band across the sleep episode--did not differ for derivations or groups. These results indicate that the nocturnal dynamics of sleep homeostasis are independent of derivation and remain stable across puberty.     

Event-related activity and phase locking during a psychomotor vigilance task over the course of sleep deprivation

There is profound knowledge that sleep restriction increases tonic (event‐unrelated) electroencephalographic (EEG) activity. In the present study we focused on time‐locked activity by means of phasic (event‐related) EEG analysis during a psychomotor vigilance task (PVT) over the course of sleep deprivation. Twenty healthy subjects (10 male; mean age ± SD: 23.45 ± 1.97 years) underwent sleep deprivation for 24 h. Subjects had to rate their sleepiness hourly (Karolinska Sleepiness Scale) and to perform a PVT while EEG was recorded simultaneously. Tonic EEG changes in the δ (1–4 Hz), θ (4–8 Hz) and α (8–12 Hz) frequency range were investigated by power spectral analyses. Single‐trial (phase‐locking index, PLI) and event‐related potential (ERP) analyses (P1, N1) were used to examine event‐related changes in EEG activity. Subjective sleepiness, PVT reaction times and tonic EEG activity (delta and theta spectral power) significantly increased over the night. In contrast, event‐related EEG parameters decreased throughout sleep deprivation. Specifically, the ERP component P1 diminished in amplitude, and delta and theta PLI estimates decreased progressively over the night. It is suggested that event‐related EEG measures (such as the amplitude of the P1 and especially delta/theta phase‐locking) serve as a complimentary method to track the deterioration of attention and performance during sleep loss. As these measures actually reflect the impaired response to specific events rather than tonic changes during sleep deprivation they are a promising tool for future sleep research.     

Effects of sleep restriction on the sleep electroencephalogram of adolescents

Study ObjectivesThis report describes findings from an ongoing longitudinal study of the effects of varied sleep durations on wake and sleep electroencephalogram (EEG) and daytime function in adolescents. Here, we focus on the effects of age and time in bed (TIB) on total sleep time (TST) and nonrapid eye movement (NREM) and rapid eye movement (REM) EEG.MethodsWe studied 77 participants (41 male) ranging in age from 9.9 to 16.2 years over the 3 years of this study. Each year, participants adhered to each of three different sleep schedules: four consecutive nights of 7, 8.5, or 10 h TIB.ResultsAltering TIB successfully modified TST, which averaged 406, 472 and 530 min on the fourth night of 7, 8.5, and 10 h TIB, respectively. As predicted by homeostatic models, shorter sleep durations produced higher delta power in both NREM and REM although these effects were small. Restricted sleep more substantially reduced alpha power in both NREM and REM sleep. In NREM but not REM sleep, sleep restriction strongly reduced both the all-night accumulation of sigma EEG activity (11–15 Hz energy) and the rate of sigma production (11–15 Hz power).ConclusionsThe EEG changes in response to TIB reduction are evidence of insufficient sleep recovery. The decrease in sigma activity presumably reflects depressed sleep spindle activity and suggests a manner by which sleep restriction reduces waking cognitive function in adolescents. Our results thus far demonstrate that relatively modest TIB manipulations provide a useful tool for investigating adolescent sleep biology.     

Topographic mapping of EEG during sleep

Summary Topographic aspects of all night sleep EEG were investigated in 10 healthy volunteers (age 20–35 years). EEG brain maps showed an increase of delta power from stage 1 to 4, a decrease of alpha power most pronounced parieto-occipitally and a slowing of the dominant alpha frequency. Differences of EEG power in different sleep stages (as compared to wakefulness) are displayed topographically. Analysis of the course of stage 2 showed an increase of delta power and a decrease of theta power in the first sections of the night, and an increase of beta power later in the night.     

Developmental changes in the sleep electroencephalogram of adolescent boys and girls

The sleep electroencephalogram (EEG) changes across adolescence; however, there are conflicting data as to whether EEG changes are regionally specific, are evident in non‐rapid eye movement (NREM) and rapid eye movement (REM) sleep, and whether there are sex differences. The present study seeks to resolve some of these issues in a combined cross‐sectional and longitudinal analysis of sleep EEG in adolescents. Thirty‐three healthy adolescents (18 boys, 15 girls; 11–14 years) were studied on two occasions 6–8 months apart. Cross‐sectional analysis of data from the initial visit revealed significantly less slow‐wave sleep, delta (0.3 to <4 Hz) and theta (4 to <8 Hz) power in both NREM and REM sleep with advancing age. The age–delta power relationship was significant at the occipital site, with age accounting for 26% of the variance. Longitudinal analysis revealed that NREM delta power declined significantly from the initial to follow‐up visit, in association with declining delta amplitude and incidence (P < 0.01), with the effect being greatest at the occipital site. REM delta power also declined over time in association with reduced amplitude (P < 0.01). There were longitudinal reductions in theta, alpha and sigma power in NREM and REM sleep evident at the occipital site at follow‐up (P < 0.01). No sex differences were apparent in the pattern of change with age for NREM or REM sleep. Declines in sleep EEG spectral power occur across adolescence in both boys and girls, particularly in the occipital derivation, and are not state‐specific, occurring in both NREM and REM sleep.     

Sympathetic overactivity and plasma leptin levels in Rett syndrome

The authors examined electroencephalographic (EEG) oscillatory responses to two violent events, the player character wounding and killing an opponent character with a gun, in the digital game James Bond 007: NightFire. EEG was recorded from 25 (16 male) right-handed healthy young adults. EEG data were segmented into one 1-s baseline epoch before each event and two 1-s epochs after event onset. Power estimates (microV(2)) were derived with the fast Fourier transform (FFT) for each artefact free event. Both of the studied events evoked increased occipital theta (4-6Hz) responses as compared to the pre-event baseline. The wounding event evoked also increased occipital high theta (6-8Hz) response and the killing event evoked low alpha (8-10Hz) asymmetry over the central electrodes, both relative to the pre-event baseline. The results are discussed in light of facial electromyographic and electrodermal activity responses evoked by these same events, and it is suggested that the reported EEG responses may be attributable to affective processes related to these violent game events.     

Cross-correlation of EEG frequency bands and heart rate variability for sleep apnoea classification

Sleep apnoea is a sleep breathing disorder which causes changes in cardiac and neuronal activity and discontinuities in sleep pattern when observed via electrocardiogram (ECG) and electroencephalogram (EEG). Using both statistical analysis and Gaussian discriminative modelling approaches, this paper presents a pilot study of assessing the cross-correlation between EEG frequency bands and heart rate variability (HRV) in normal and sleep apnoea clinical patients. For the study we used EEG (delta, theta, alpha, sigma and beta) and HRV (LF_nu, HF_nu and LF/HF) features from the spectral analysis. The statistical analysis in different sleep stages highlighted that in sleep apnoea patients, the EEG delta, sigma and beta bands exhibited a strong correlation with HRV features. Then the correlation between EEG frequency bands and HRV features were examined for sleep apnoea classification using univariate and multivariate Gaussian models (UGs and MGs). The MG outperformed the UG in the classification. When EEG and HRV features were combined and modelled with MG, we achieved 64% correct classification accuracy, which is 2 or 8% improvement with respect to using only EEG or ECG features. When delta and acceleration coefficients of the EEG features were incorporated, then the overall accuracy improved to 71%.     

Habitual napping moderates motor performance improvements following a short daytime nap

The effect of napping on motor performance was examined in habitual and non-habitual nappers who were randomly assigned to a nap or reading condition. Motor procedural learning and auditory discrimination tasks were administered pre- and post-condition. Both groups reported improved alertness post-nap, but not post-reading. Non-habitual nappers fell asleep faster and tended to have greater sleep efficiency, but did not differ from habitual nappers on other sleep architecture variables. Habitual nappers had greater alpha and theta EEG power in stage 1, and greater delta, alpha and sigma power in stage 2 sleep. Motor performance deteriorated for non-habitual nappers who napped, but improved for all others. The number of sleep spindles and sigma power (13.5-15 Hz) significantly predicted motor performance following the nap, for habitual nappers only. Results indicate that motor learning was consolidated in a brief nap and was associated with stage 2 spindles, but only for those who habitually take naps.     

Analysis of slow-wave activity and slow-wave oscillations prior to somnambulism

Study Objectivies:

Several studies have investigated slow wave sleep EEG parameters, including slow-wave activity (SWA) in relation to somnambulism, but results have been both inconsistent and contradictory. The first goal of the present study was to conduct a quantitative analysis of sleepwalkers'' sleep EEG by studying fluctuations in spectral power for delta (1-4 Hz) and slow delta (0.5-1 Hz) before the onset of somnambulistic episodes. A secondary aim was to detect slow-wave oscillations to examine changes in their amplitude and density prior to behavioral episodes.

Participants:

Twenty-two adult sleepwalkers were investigated polysomnographically following 25 h of sleep deprivation.

Results:

Analysis of patients'' sleep EEG over the 200 sec prior to the episodes'' onset revealed that the episodes were not preceded by a gradual increase in spectral power for either delta or slow delta over frontal, central, or parietal leads. However, time course comparisons revealed significant changes in the density of slow-wave oscillations as well as in very slow oscillations with significant increases occurring during the final 20 sec immediately preceding episode onset.

Conclusions:

The specificity of these sleep EEG parameters for the occurrence and diagnosis of NREM parasomnias remains to be determined.

Citation:

Jaar O; Pilon M; Carrier J; Montplaisir J; Zadra A. Analysis of slow-wave activity and slow-wave oscillations prior to somnambulism. SLEEP 2010;33(11):1511-1516.