Abstract
Sleep and wakefulness are traditionally considered as two mutually exclusive states with contrasting behavioural manifestations and complementary neurobiological functions. However, the discoveries of local sleep in global wakefulness and local wakefulness in global sleep have challenged this classical view and raised questions about the nature and functions of sleep. Here, we review the contributions from recent multimodal imaging studies of human sleep towards understanding the relationship between the nature and functions of sleep. Through simultaneous tracking of brain state and mapping of brain activity, these studies revealed that the sleeping brain can carry out covert cognitive processing that was thought to be wake-specific (wake-like function in the sleeping brain). Conversely, the awake brain can perform housekeeping functions through local sleep of neural populations (sleep-like function in the awake brain). We discuss how the blurred boundary between sleep and wakefulness highlights the need to radically rethink the definition of brain states, and how the recently discovered fMRI signatures of global and local sleep can help to address these outstanding questions.
Highlights
Sleep is a state of behavioural quiescence, characterized by sensory-motor disconnection from the environment, and reduced levels of responsiveness and consciousness [1,2]
It was discovered that the level of brain metabolism is similar between wake and rapid eye movement (REM) sleep and reduced by only 20% from wake to non-rapid eye movement (NREM) sleep [3,4], suggesting that the sleeping brain is highly active
Functional magnetic resonance imaging provides the fine spatial resolution and whole brain coverage required for recording local brain activity
Summary
Sleep is a state of behavioural quiescence, characterized by sensory-motor disconnection from the environment, and reduced levels of responsiveness and consciousness [1,2]. To study the relationship between the nature and functions of human sleep, a technical challenge lies in the simultaneous tracking of global brain state and recording of local brain activity. EEG has good temporal resolution and can detect rapid changes in global brain state, its spatial resolution is limited. Functional magnetic resonance imaging (fMRI) provides the fine spatial resolution and whole brain coverage required for recording local brain activity. FMRI blood-oxygen-level-dependent (BOLD) signal reflects localized changes in brain blood flow and blood oxygenation, which are driven by neural activity through neurovascular coupling [10]. Given the constraints of individual brain imaging techniques, a number of studies have applied a multimodal imaging approach, such as combined EEG-fMRI, to simultaneously track global brain state and record local brain activity during human sleep [12]
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