Temporal Dynamics of Brain Integration During Sleep and Arousal Shifts

Review Article

Temporal Dynamics of Brain Integration During Sleep and Arousal Shifts

Aino Virtanen¹* and Jari Lehtinen²

¹Department of Clinical Genetics, University of Helsinki, Helsinki, Finland
2Department of Neuroscience, University of Eastern Finland, Kuopio, Finland

Published: 14 April 2020

Abstract

Sleep is a fundamental physiological process characterized by profound changes in brain activity and behavior. Beyond the well-established Electroencephalographic (EEG) patterns defining sleep stages, understanding how different brain regions interact and synchronize – i.e., integrative brain activity or functional connectivity – is crucial for elucidating the functional significance of sleep. This review synthesizes findings on the characteristics of integrative brain activity across wakefulness, the distinct stages of non-rapid eye movement (NREM) sleep (N1, N2, N3/slow-wave sleep), Rapid Eye Movement (REM) sleep, and the dynamic transitions between these states. Studies employing techniques such as EEG coherence, source localization, Functional Magnetic Resonance Imaging (fMRI), and Magnetoencephalography (MEG) have revealed state-dependent changes in large-scale brain networks, including the Default Mode Network (DMN), salience network, and executive control network. Wakefulness is characterized by complex, dynamic network interactions. NREM sleep, particularly N3, is associated with widespread slow-wave activity and a fragmentation or decoupling of some large-scale networks, alongside localized increases in connectivity potentially related to memory processing (e.g., hippocampal-cortical interactions during spindles). REM sleep presents a unique profile with reduced connectivity in prefrontal areas but increased connectivity within limbic and paralimbic systems. Transitional states exhibit highly dynamic and sometimes unstable patterns of connectivity, reflecting the shift between distinct network configurations. Investigating integrative activity provides insights into the mechanisms underlying consciousness, sensory processing, memory consolidation, and the vulnerability to state misperception during sleep and transitions. Future research directions include combining high-temporal resolution methods with causal manipulations and sophisticated network analysis techniques to better understand the causal roles of specific network dynamics.

Keywords: Sleep stages; NREM sleep; REM sleep; Wakefulness; Brain connectivity; Functional networks; EEG coherence; fMRI; Transitional states; Memory consolidation; Consciousness