The two-process model of sleep regulation: a reappraisal

Abstract The high prevalence of chronic sleep restriction in adolescents underscores the importance of understanding how adolescent sleep is regulated under such conditions. One component of sleep regulation is a homeostatic process: if sleep is restricted, then sleep intensity increases. Our knowledge of this process is primarily informed by total sleep deprivation studies and has been incorporated in mathematical models of human sleep regulation. Several animal studies, however, suggest that adaptation occurs in chronic sleep restriction conditions, showing an attenuated or even decreased homeostatic response. We investigated the homeostatic response of adolescents to different sleep opportunities. Thirty-four participants were allocated to one of three groups with 5, 7.5 or 10 h of sleep opportunity per night for 5 nights. Each group underwent a protocol of 9 nights designed to mimic a school week between 2 weekends: 2 baseline nights (10 h sleep opportunity), 5 condition nights (5, 7.5 or 10 h), and two recovery nights (10 h). Measures of sleep homeostasis (slow-wave activity and slow-wave energy) were calculated from frontal and central EEG derivations and compared to predictions derived from simulations of the homeostatic process of the two-process model of sleep regulation. Only minor differences were found between empirical data and model predictions, indicating that sleep homeostasis is preserved under chronic sleep restriction in adolescents. These findings improve our understanding of effects of repetitive short sleep in adolescents.

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Circadian Rhythms and Homeostatic Mechanisms for Sleep Regulation

Integrative Sleep Medicine ◽

10.1093/med/9780190885403.003.0005 ◽

2021 ◽

pp. 65-86

Author(s):

Cassie J. Hilditch ◽

Erin E. Flynn-Evans

Keyword(s):

Circadian Rhythm ◽

Circadian Rhythms ◽

Process Model ◽

Modern Society ◽

Current Evidence ◽

Sleep Regulation ◽

Sleep Homeostasis ◽

Short And Long Term ◽

Homeostatic Mechanisms

This chapter examines circadian rhythms and homeostatic mechanisms for sleep regulation. It reviews the current evidence describing the two-process model of sleep regulation and how to assess disruption to either of these sleep drives. This chapter also reviews the role of the photic and non-photic resetting of the circadian rhythm and describes how some aspects of modern society can cause sleep and circadian disruption. Further, this chapter describes how misalignment between the circadian rhythm and sleep homeostasis, such as occurs during jet lag and shift-work, can lead to sleep disruption. The short- and long-term consequences of circadian misalignment are also reviewed.

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Glymphatic Dysfunction: A Bridge Between Sleep Disturbance and Mood Disorders

Frontiers in Psychiatry ◽

10.3389/fpsyt.2021.658340 ◽

2021 ◽

Vol 12 ◽

Author(s):

Tao Yan ◽

Yuefeng Qiu ◽

Xinfeng Yu ◽

Linglin Yang

Keyword(s):

Sleep Disturbance ◽

Mood Disorders ◽

Process Model ◽

Water Channel ◽

Sleep Regulation ◽

Sleep Homeostasis ◽

Close Relationship ◽

Mechanism Of Interaction ◽

Glymphatic Pathway ◽

Dynamic Fluctuation

Mounting evidence demonstrates a close relationship between sleep disturbance and mood disorders, including major depression disorder (MDD) and bipolar disorder (BD). According to the classical two-process model of sleep regulation, circadian rhythms driven by the light–dark cycle, and sleep homeostasis modulated by the sleep–wake cycle are disrupted in mood disorders. However, the exact mechanism of interaction between sleep and mood disorders remains unclear. Recent discovery of the glymphatic system and its dynamic fluctuation with sleep provide a plausible explanation. The diurnal variation of the glymphatic circulation is dependent on the astrocytic activity and polarization of water channel protein aquaporin-4 (AQP4). Both animal and human studies have reported suppressed glymphatic transport, abnormal astrocytes, and depolarized AQP4 in mood disorders. In this study, the “glymphatic dysfunction” hypothesis which suggests that the dysfunctional glymphatic pathway serves as a bridge between sleep disturbance and mood disorders is proposed.

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Homeostatic sleep regulation in habitual short sleepers and long sleepers

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1996.270.1.r41 ◽

1996 ◽

Vol 270 (1) ◽

pp. R41-R53 ◽

Cited By ~ 15

Author(s):

D. Aeschbach ◽

C. Cajochen ◽

H. Landolt ◽

A. A. Borbely

Keyword(s):

Rem Sleep ◽

Process Model ◽

Sleep Latency ◽

Spectral Power ◽

Spectral Power Density ◽

Sleep Time ◽

Sleep Regulation ◽

Sleep Episode ◽

Rem Density ◽

Electroencephalogram Eeg

Homeostatic sleep regulation in habitual short sleepers (sleep episode < 6 h, n = 9) and long sleepers (> 9 h, n = 7) was investigated by studying their sleep structure and sleep electroencephalogram (EEG) during baseline conditions and after prolonging their habitual waking time by 24 h. In each sleep episode, total sleep time was > 3 h longer in the long sleepers than in the short sleepers. Sleep deprivation decreased sleep latency and rapid eye movement (REM) density in REM sleep more in long sleepers than in short sleepers. The enhancement of EEG slow-wave activity (SWA; spectral power density in the 0.75-4.5 Hz range) in non-REM sleep after sleep loss was larger in long sleepers (47%) than in short sleepers (19%). This difference in the SWA response was predicted by the two-process model of sleep regulation on the basis of the different sleep durations. The results indicate that short sleepers live under a higher “non-REM sleep pressure” than long sleepers. However, the two groups do not differ with respect to the homeostatic sleep regulatory mechanisms.

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Bright morning light advances the human circadian system without affecting NREM sleep homeostasis

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1989.256.1.r106 ◽

1989 ◽

Vol 256 (1) ◽

pp. R106-R111 ◽

Cited By ~ 13

Author(s):

D. J. Dijk ◽

D. G. Beersma ◽

S. Daan ◽

A. J. Lewy

Keyword(s):

Rem Sleep ◽

Process Model ◽

Sleep Onset ◽

Light Condition ◽

Bright Light ◽

Circadian Pacemaker ◽

Sleep Regulation ◽

Plasma Melatonin ◽

Sleep Homeostasis ◽

Dim Light

Eight male subjects were exposed to either bright light or dim light between 0600 and 0900 h for 3 consecutive days each. Relative to the dim light condition, the bright light treatment advanced the evening rise in plasma melatonin and the time of sleep termination (sleep onset was held constant) for an average approximately 1 h. The magnitude of the advance of the plasma melatonin rise was dependent on its phase in dim light. The reduction in sleep duration was at the expense of rapid-eye-movement (REM) sleep. Spectral analysis of the sleep electroencephalogram (EEG) revealed that the advance of the circadian pacemaker did not affect EEG power densities between 0.25 and 15.0 Hz during either non-REM or REM sleep. The data show that shifting the human circadian pacemaker by 1 h does not affect non-REM sleep homeostasis. These findings are in accordance with the predictions of the two-process model of sleep regulation.

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Time course of EEG power density during long sleep in humans

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1990.258.3.r650 ◽

1990 ◽

Vol 258 (3) ◽

pp. R650-R661 ◽

Cited By ~ 10

Author(s):

D. J. Dijk ◽

D. P. Brunner ◽

A. A. Borbely

Keyword(s):

Slow Wave ◽

Process Model ◽

Time Course ◽

Slow Wave Sleep ◽

Nrem Sleep ◽

Sleep Stages ◽

Base Line ◽

Sleep Regulation ◽

Recovery Sleep ◽

Electroencephalogram Eeg

In nine subjects sleep was recorded under base-line conditions with a habitual bedtime (prior wakefulness 16 h; lights off at 2300 h) and during recovery from sleep deprivation with a phase-advanced bedtime (prior wakefulness 36 h; lights off at 1900 h). The duration of phase-advanced recovery sleep was greater than 12 h in all subjects. Spectral analysis of the sleep electroencephalogram (EEG) revealed that slow-wave activity (SWA; 0.75-4.5 Hz) in non-rapid-eye-movement (NREM) sleep was significantly enhanced during the first two NREM-REM sleep cycles of displaced recovery sleep. The sleep stages 3 and 4 (slow-wave sleep) and SWA decreased monotonically over the first three and four NREM-REM cycles of, respectively, base-line and recovery sleep. The time course of SWA in base-line and recovery sleep could be adequately described by an exponentially declining function with a horizontal asymptote. The results are in accordance with the two-process model of sleep regulation in which it is assumed that SWA rises as a function of the duration of prior wakefulness and decreases exponentially as a function of prior sleep. We conclude that the present data do not provide evidence for a 12.5-h sleep-dependent rhythm of deep NREM sleep.

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Topography of EEG Dynamics After Sleep Deprivation in Mice

Journal of Neurophysiology ◽

10.1152/jn.2000.84.4.1888 ◽

2000 ◽

Vol 84 (4) ◽

pp. 1888-1893 ◽

Cited By ~ 89

Author(s):

Reto Huber ◽

Tom Deboer ◽

Irene Tobler

Keyword(s):

Sleep Deprivation ◽

Time Constant ◽

Frequency Band ◽

Regional Differences ◽

Process Model ◽

Nrem Sleep ◽

Occipital Cortex ◽

Brain Regions ◽

Prior History ◽

Sleep Regulation

Several recent results show that sleep and sleep regulation are not only global phenomena encompassing the entire brain, but have local features. It is well established that slow-wave activity [SWA; mean electroencephalographic (EEG) power density in the 0.75–4.0 Hz band] in non–rapid eye movement (NREM) sleep is a function of the prior history of sleep and wakefulness. SWA is thought to reflect the homeostatic component of the two-process model of sleep regulation. According to this model, originally formulated for the rat and later extended to human sleep, the timing and structure of sleep are determined by the interaction of a homeostatic Process S and a circadian process. Our aim was to investigate the dynamics of SWA in the EEG of two brain regions (frontal and occipital cortex) after sleep deprivation (SD) in two of the mice strains most often used in gene targeting. C57BL/6J ( n = 9) and 129/Ola ( n = 8) were recorded during a 24-h baseline day, 6-h SD, and 18-h recovery. Both derivations showed a significant increase in SWA in NREM sleep after SD in both strains. In the first hour of recovery, SWA was enhanced more in the frontal derivation than in the occipital derivation and showed a faster decline. This difference resulted in a lower value for the time constant for the decrease of SWA in the frontal derivation (frontal: 10.9 ± 2.1 and 6.8 ± 0.9 h in Ola and C57, respectively; occipital: 16.6 ± 2.1 and 14.1 ± 1.5 h; P < 0.02; for each of the strains; paired t-test). Neither time constant differed significantly between the strains. The subdivision of SWA into a slower and faster band (0.75–2.5 Hz and 2.75–4.0 Hz) further highlighted regional differences in the effect of SD. The lower frequency band had a higher initial value in the frontal derivation than in the occipital derivation in both strains. Moreover, in the higher frequency band a prominent reversal took place so that power in the frontal derivation fell below the occipital values in both strains. Thus our results indicate that there may be differences in the brain in the effects of SD on SWA in mice, suggesting regional differences in the dynamics of the homeostatic component of sleep regulation. The data support the hypothesis that sleep has local, use- or waking-dependent features that are reflected in the EEG, as has been shown for humans and the laboratory rat.

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