Sleep defined by arousal threshold reveals decreases in corticocortical functional correlations independently from the conventional sleep stages

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Abstract

Sleep research and sleep medicine have benefited from the use of polysomnography but have also suffered from an overreliance on the conventional, polysomnography-defined sleep stages. For example, reports of sleep-specific brain activity patterns have, with few exceptions, been constrained by assessing brain function as it relates to the conventional sleep stages. This limits the variety of sleep states and underlying activity patterns that one can discover. If undiscovered brain activity patterns exist during sleep, then removing the constraint of a stage-specific analysis may uncover them. The current study used all-night functional magnetic resonance imaging sleep data and defined sleep behaviorally with auditory arousal threshold (AAT) to begin to search for new brain states. It was hypothesized that, during sleep compared to wakefulness, corticocortical functional correlations would decrease. Functional correlation values calculated in a window immediately before the determination of AAT were entered into a linear mixed effects model, allowing multiple arousals across the night per subject into the analysis. The hypothesis was supported using both correlation matrices of brain networks and single seed-region analyses showing whole-brain maps. This represents a novel approach to studying the neuroanatomical correlates of sleep with high spatial resolution by defining sleep in a way that was independent from the conventional sleep stages. This work provides initial evidence to justify searching for sleep stages that are more neuroanatomically localized and unrelated to the conventional sleep stages.

Statement of Significance

Conventional sleep stages were established because they correlated with the original behavioral characteristics of sleep, most notably, arousal threshold. With the proliferation of new techniques to measure the brain during sleep, the first experiments might have been to perform correlations with arousal threshold. These experiments have never been performed, either with functional magnetic resonance imaging (MRI) or with any other modern technique. To begin to search for new sleep stages, the amount of communication between brain regions as measured by all-night functional MRI was correlated with arousal threshold. Communication between brain regions decreased as sleep depth, measured behaviorally, increased. This provides initial evidence to justify searching for sleep stages that are unrelated to the conventional sleep stages.

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