Waking experience modulates sleep need in mice

Abstract

Background Homeostatic regulation of sleep is reflected in the maintenance of a daily balance between sleep and wakefulness. Although numerous internal and external factors can influence sleep, it is unclear whether and to what extent the process that keeps track of time spent awake is determined by the content of the waking experience. We hypothesised that alterations in environmental conditions may elicit different types of wakefulness, which will in turn influence both the capacity to sustain continuous wakefulness as well as the rates of accumulating sleep pressure. To address this, we compared the effects of repetitive behaviours such as voluntary wheel running or performing a simple touchscreen task, with wakefulness dominated by novel object exploration, on sleep timing and EEG slow-wave activity (SWA) during subsequent NREM sleep. Results We find that voluntary wheel running is associated with higher wake EEG theta-frequency activity and results in longer wake episodes, as compared with exploratory behaviour; yet, it does not lead to higher levels of EEG SWA during subsequent NREM sleep in either the frontal or occipital derivation. Furthermore, engagement in a touchscreen task, motivated by food reward, results in lower SWA during subsequent NREM sleep in both derivations, as compared to exploratory wakefulness, even though the total duration of wakefulness is similar. Conclusion Overall, our study suggests that sleep-wake behaviour is highly flexible within an individual and that the homeostatic processes that keep track of time spent awake are sensitive to the nature of the waking experience. We therefore conclude that sleep dynamics are determined, to a large degree, by the interaction between the organism and the environment.

Roles for Sleep in Neural and Behavioral Plasticity: Reviewing Variation in the Consequences of Sleep Loss

“…Although sleep's physiological functions remain poorly understood, sleep loss has been associated with deleterious effects on health and cognition (Rechtschaffen and Bergmann, 1995 ; Dinges et al, 1997 ; Durmer and Dinges, 2005 ; Spiegel et al, 2005 ; Banks and Dinges, 2007 ; Knutson et al, 2007 ; Grandner et al, 2010 ). Sleep varies based on previous waking experience (Ganguly-Fitzgerald et al, 2006 ; Huber et al, 2007 ; Hanlon et al, 2009 ; Keene et al, 2010 ; Beckwith et al, 2017 ; Kirszenblat et al, 2019 ; Milinski et al, 2021 ) throughout the lifespan (Roffwarg et al, 1966 ; Kales et al, 1967 ; Feinberg and Carlson, 1968 ; Cauter et al, 2000 ; Backhaus et al, 2007 ; Dijk et al, 2010 ; Feinberg and Campbell, 2010 ; Carrier et al, 2011 ; Vienne et al, 2016 ; Mander et al, 2017 ), and between species (Lyamin et al, 2008 , 2017 , 2018 ; Siegel, 2008 ; Lesku et al, 2012 ), suggesting that sleep has multiple functions. However, because sleep coincides with broad changes in neurophysiology and necessitates a loss of consciousness with reduced responsiveness to external threats, it is likely that sleep evolved, at least in part, to support brain function (Rasch and Born, 2013 ; Tononi and Cirelli, 2014 ).…”

Sound disrupts sleep-associated brain oscillations in rodents in a meaning-dependent manner

“…During the experiment, we used online visual inspection, based on conventional criteria in sleep scoring 27 , 28 , of the ongoing oscillations to categorize the current vigilance state as awake, REM, NREM, or unidentifiable. To ensure that this decision matched a quantifiable measure, we first compared the manual scoring with a quantitative analysis of the corresponding EEG spectra.…”

The hypothalamic link between arousal and sleep homeostasis in mice

“…Taken together with optical activation experiments, we speculate on the role of these neurons as follows. When the population of GAD2 LPO neurons is spontaneously active, which may be driven indirectly by external stimuli through inputs from other brain areas, such as hypocretin/orexin, noradrenaline, or cortical/striatal neurons (17,41,89,90), the animals engage in wakefulness characterized by increased levels of activity and arousal, and this leads to a subsequent increase in sleep intensity (49,61). This is increased further in already awake animals if the activity of these neurons is artificially enhanced by optostimulation, while rapid awakening occurs when stimulation is delivered during sleep.…”