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Towards an Embodied Account of Sleep Loss

Abstract

Sleep is fundamental to life. Multiple biological functions, from peripheral immune and cardiovascular systems, to central brain operations governing cognition and emotion, are perturbed by sleep when deficient and restored by sleep when sufficient. This evidence leads to the proposition that sleep is necessary for coordinating whole-organism adaptation, which requires the active co-regulation of both brain and body systems for optimal physiological stability during stress, termed allostasis. Although causal links within and between the brain and body are recognized as essential, a multi-system examination of these interactions under conditions of insufficient sleep has yet to be reported. Elucidating the interdependence of the multi-system impacts of sleep loss is not only necessary to build a deeper understanding of the function of sleep, but also to guide informed treatments for a number of chronic diseases characterized by both sleep disturbances and multi-system etiology, such as chronic pain and cardiovascular disease. This thesis combines functional magnetic resonance brain imaging with measurements of peripheral physiological function in order to test the overarching hypothesis that the dysfunction observed across multiple brain and body systems under conditions of sleep loss are intimately interrelated, rather than independent. Three specific aims emerge from this hypothesis and are addressed in this thesis: (1) The first aim sets forth the hypothesis that sleep loss impairs the function and architecture of brain networks with consequences for cognition, affect, and physiology. A comprehensive review of neuroimaging studies of sleep deprivation in humans demonstrates that sleep loss alters the architecture of human brain networks, and with it, the processes dependent on these networks. Many of the brain regions and networks most impacted by sleep deprivation are affective and viscerosensory brain regions involved in the master regulation of allostasis. (2) The second aim addresses the hypothesis that, in addition to the central brain, sleep loss impairs the functioning of peripheral adaptive systems and that central and peripheral dysfunction are interrelated, focusing on the immune system and pain. An experimental sleep deprivation study in humans demonstrates that sleep deprivation increases levels of circulating pro-inflammatory cytokines, and that this pro-inflammatory state contributes to increased pain perception assessed both objectively in the brain and subjectively through participant ratings. (3) The third aim tests the hypothesis that interrelated dysfunction in the brain and the body is evident in a different model system involved in allostasis, the cardiovascular system. A second sleep deprivation experiment establishes significant interdependence between sleep loss-increased blood pressure, disruption of central brain viscerosensory networks, and worse mood state. Collectively, these results support an embodied framework of sleep loss wherein sleep loss contributes to disease through a disruption of the brain-body coordination required for allostasis. Considering the continual erosion of sleep across society, these findings hold important scientific, clinical and public health implications.

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