Prolonged Exposure to Social Stress Impairs Homeostatic Sleep Regulation.

Basma Radwan,Soaad Hammami,Dipesh Chaudhury,Alvaro Yanez Touzet

doi:10.3389/fnins.2021.633955

Basma Radwan, Soaad Hammami + Show 2 more

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https://doi.org/10.3389/fnins.2021.633955

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Abstract

Stress and sleep are tightly regulated as a result of the substantial overlap in neurotransmitter signaling and regulatory pathways between the neural centers that modulate mood and sleep-wake cycle. The chronicity of the stressor and variability in coping with it are major determinants of the psychiatric outcomes and subsequent effect on sleep. The regulation of sleep is mediated by the interaction of a homeostatic and a circadian process according to the two-process model. Chronic stress induces stress-related disorders which are associated with deficient sleep homeostasis. However, little is known about how chronic stress affects sleep homeostasis and whether the differences in adaptation to stress distinctively influence sleep. Therefore, we assessed sleep homeostasis in C57BL6/J mice following exposure to 15-d of chronic social defeat stress. We implemented wake:sleep ratio as a behavioral correlate of sleep pressure. Both stress-resilient and stress-susceptible mice displayed deficient sleep homeostasis in post-stress baseline sleep. This was due to poor temporal correlation between frontal slow wave activity (SWA) power and sleep pressure in the dark/active phase. Moreover, the buildup rate of sleep pressure in the dark was lower in susceptible mice in comparison to stress-naïve mice. Additionally, 4-h SD in the dark caused a deficient sleep recovery response in susceptible mice characterized by non-rapid eye movement (NREM) sleep loss. Our findings provide evidence of deficient homeostatic sleep process (S) in baseline sleep in stress-exposed mice, while impaired sleep recovery following a mild enforced wakefulness experienced during the dark was only detected in stress-susceptible mice. This alludes to the differential homeostatic adaptation to stress between susceptible and resilient mice and its effect on sleep regulation.

Highlights

Sleep is ubiquitous across many diverse species such as vertebrates, arthropods, nematodes and even Cassiopea jellyfish which lack a centralized nervous system (Nath et al, 2017)
Frontal and parietal slow wave activity (SWA) in stress-naïve mice gradually increased during the early dark cycle and peaked around ZT20 (p = 0.001 and p = 0.005), after which they started declining toward the end of the dark cycle and remained low during the light cycle when the sleep pressure is low due to greater amount of sleep relative to wake (Figure 2B bottom)
Since SWA of non-rapid eye movement (NREM) sleep is a proxy for sleep homeostasis and a functional correlate of sleep pressure, we hypothesized that the increase in SWA power from early- to late-dark period should be consistent with the increase in sleep pressure, during the regular waking hours of mice in the dark

Summary

Introduction

Sleep is ubiquitous across many diverse species such as vertebrates, arthropods, nematodes and even Cassiopea jellyfish which lack a centralized nervous system (Nath et al, 2017). Sleep homeostasis is strongly correlated with slow wave activity (SWA) with frequencies ranging between 0.5 and 4.5 Hz during NREM sleep (Deboer, 2007). The transitions between the up and down states are associated with cortical slow waves and prolonged duration of the down state leads to greater SWA power (Steriade et al, 2001; Battaglia et al, 2004; Vyazovskiy and Faraguna, 2015; Levenstein et al, 2019). It is well established that slow waves (SWs) mediate the synaptic downscaling possibly associated with the renormalization of synapses during sleep (Levenstein et al, 2017; Norimoto et al, 2018; Tononi and Cirelli, 2019)

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