Abstract
Twenty-four hour rhythms of physiology and behavior are driven by the environment and an internal endogenous timing system. Daily restricted feeding (RF) in nocturnal rodents during their inactive phase initiates food anticipatory activity (FAA) and a reorganization of the typical 24-hour sleep–wake structure. Here, we investigate the effects of daytime feeding, where food access was restricted to 4 hours during the light period ZT4-8 (Zeitgeber time; ZT0 is lights on), on sleep–wake architecture and sleep homeostasis in mice. Following 10 days of RF, mice were returned to ad libitum feeding. To mimic the spontaneous wakefulness associated with FAA and daytime feeding, mice were then sleep deprived between ZT3-6. Although the amount of wake increased during FAA and subsequent feeding, total wake time over 24 hours remained stable as the loss of sleep in the light phase was compensated for by an increase in sleep in the dark phase. Interestingly, sleep that followed spontaneous wake episodes during the dark period and the extended period of wake associated with FAA, exhibited lower levels of slow-wave activity (SWA) when compared to baseline or after sleep deprivation, despite a similar duration of waking. This suggests an evolutionary mechanism of reducing sleep drive during negative energy balance to enable greater arousal for food-seeking behaviors. However, the total amount of sleep and SWA accumulated during the 24 hours was similar between baseline and RF. In summary, our study suggests that despite substantial changes in the daily distribution and quality of wake induced by RF, sleep homeostasis is maintained.
Highlights
Patterns in behavioral and physiological state emerge through the actions of an intrinsic circadian timekeeping system and its synchronization to recurrent environmental signals or Zeitgebers [1]
Analysis of EEG spectra recorded during waking, non-rapid eye movement sleep (NREM) sleep, and rapid eye movement sleep (REM) sleep (Figure 1D) revealed a distribution of spectral power across frequencies in the frontal and occipital derivations that is characteristic for mice [10]
To evaluate how animals adapted to this temporal perturbation in food availability, the amount of waking in the 2 hours preceding the presentation of food was quantified over 10 successive days of restricted feeding (RF) to encompass the period where animals typically showed food anticipatory activity (FAA)
Summary
Patterns in behavioral and physiological state emerge through the actions of an intrinsic circadian timekeeping system and its synchronization to recurrent environmental signals or Zeitgebers [1]. Variation in environmental light is the dominant Zeitgeber where photic information is conveyed from the eye, via the retinohypothalamic tract (RHT), to the master circadian pacemaker in the brain’s suprachiasmatic nuclei (SCN) [2]. Two key processes influenced by the SCN are the onset of sleep and patterns of food intake [3, 4] For nocturnal animals, this partitions rest and infrequent feeding activity to the day, whereas waking and frequent feeding are mostly confined to the night [5]. This partitions rest and infrequent feeding activity to the day, whereas waking and frequent feeding are mostly confined to the night [5] Both food intake and sleep are subject to strong homeostatic control that ensure appropriate amounts of daily feeding, wake duration, and sleep intensity
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