Homeostatic and Circadian Contribution to EEG and Molecular State Variables of Sleep Regulation

Mar 2, 2013Sleep

How daily rhythms and body balance affect brain waves and molecular signs of sleep regulation

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Abstract

Forebrain expression of the clock genes Per2 and Dbp in male mice is affected by time of day during elevated sleep pressure.

The expression of Per2 increased and Dbp decreased in relation to time spent awake, suggesting their involvement in sleep regulation.
Changes in Per2 and Dbp expression during sleep deprivation varied significantly with the time of day, particularly decreasing for Per2 during specific phases.
The dynamics of Dbp expression were found to be opposite to those of Per2 under similar conditions.
EEG delta power and levels of Homer1a, markers of sleep homeostasis, were influenced by sleep-wake distribution and time of day.
The increase in delta power after sleep deprivation was higher than expected when recovery sleep began at dark onset.
These findings indicate a complex interaction between circadian rhythms and homeostatic sleep processes.

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STUDY OBJECTIVES: Besides their well-established role in circadian rhythms, our findings that the forebrain expression of the clock-genes Per2 and Dbp increases and decreases, respectively, in relation to time spent awake suggest they also play a role in the homeostatic aspect of sleep regulation. Here, we determined whether time of day modulates the effects of elevated sleep pressure on clock-gene expression. Time of day effects were assessed also for recognized electrophysiological (EEG delta power) and molecular (Homer1a) markers of sleep homeostasis.

DESIGN: EEG and qPCR data were obtained for baseline and recovery from 6-h sleep deprivation starting at ZT0, -6, -12, or -18.

SETTING: Mouse sleep laboratory.

PARTICIPANTS: Male mice.

INTERVENTIONS: Sleep deprivation.

RESULTS: The sleep-deprivation induced changes in Per2 and Dbp expression importantly varied with time of day, such that Per2 could even decrease during sleep deprivations occurring at the decreasing phase in baseline. Dbp showed similar, albeit opposite dynamics. These unexpected results could be reliably predicted assuming that these transcripts behave according to a driven damped harmonic oscillator. As expected, the sleep-wake distribution accounted for a large degree of the changes in EEG delta power and Homer1a. Nevertheless, the sleep deprivation-induced increase in delta power varied also with time of day with higher than expected levels when recovery sleep started at dark onset.

CONCLUSIONS: Per2 and delta power are widely used as exclusive state variables of the circadian and homeostatic process, respectively. Our findings demonstrate a considerable cross-talk between these two processes. As Per2 in the brain responds to both sleep loss and time of day, this molecule is well positioned to keep track of and to anticipate homeostatic sleep need.

CITATION: Curie T; Mongrain V; Dorsaz S; Mang GM; Emmenegger Y; Franken P. Homeostatic and circadian contribution to EEG and molecular state variables of sleep regulation. SLEEP 2013;36(3):311-323.

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Homeostatic and Circadian Contribution to EEG and Molecular State Variables of Sleep Regulation

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