Sleep alters neurovascular and hydrodynamic coupling in the human brain
Sleep is essential for maintaining brain tissue homeostasis, which is facilitated by enhanced cerebrospinal fluid (CSF) solute transport. Infraslow (<0.1 Hz) vasomotion, CSF flow, and electrophysiological potential all increase during sleep, but their contributions as potential drivers of CSF flow in human brain remain unknown.
To investigate this, we measured these signals in healthy volunteers across sleep–wake states using functional MRI blood oxygen level-dependent (BOLD), electroencephalography, and functional near-infrared spectroscopy. We then studied the directed coupling patterns between the three signals, using phase transfer entropy.
In the awake state, electrophysiological potential and water concentration changes both predicted hemodynamic BOLD changes across whole brain, reflecting classical functional hyperemia. During sleep, these interactions changed such that the net directionality was lost and the interactions became more bidirectional.
Our results show that in addition to neural changes during sleep, nonneural processes such as vasomotor-driven hydrodynamic waves start to gain more impact on human brain activity.
SIGNIFICANCE
Beyond its well-known effects on neuronal activity, human sleep appears also to reorganize the infraslow (<0.1 Hz) oscillation hierarchy in brain. While wakefulness is dominated by unidirectional neurovascular coupling, in which neural activity predicts hemodynamic changes, our study shows that the change in brain state from wakefulness to sleep is accompanied by increased bidirectionality in prediction patterns. Sleep-related increases in signal power were associated with bidirectional prediction patterns involving electrical activity, vascular signals, and water volume changes. These multimodal findings highlight a fundamental change in coupling dependent on brain state, suggesting that both neural and nonneural alteration contribute to sleep-related brain function.
Web | DOI | PDF | Proceedings of the National Academy of Sciences | Open Access
Väyrynen, Tommi; Tuunanen, Johanna; Helakari, Heta; Elabasy, Ahmed; Korhonen, Vesa; Huotari, Niko; Piispala, Johanna; Kallio, Mika; Nedergaard, Maiken; Kiviniemi, Vesa
Sleep is essential for maintaining brain tissue homeostasis, which is facilitated by enhanced cerebrospinal fluid (CSF) solute transport. Infraslow (<0.1 Hz) vasomotion, CSF flow, and electrophysiological potential all increase during sleep, but their contributions as potential drivers of CSF flow in human brain remain unknown.
To investigate this, we measured these signals in healthy volunteers across sleep–wake states using functional MRI blood oxygen level-dependent (BOLD), electroencephalography, and functional near-infrared spectroscopy. We then studied the directed coupling patterns between the three signals, using phase transfer entropy.
In the awake state, electrophysiological potential and water concentration changes both predicted hemodynamic BOLD changes across whole brain, reflecting classical functional hyperemia. During sleep, these interactions changed such that the net directionality was lost and the interactions became more bidirectional.
Our results show that in addition to neural changes during sleep, nonneural processes such as vasomotor-driven hydrodynamic waves start to gain more impact on human brain activity.
SIGNIFICANCE
Beyond its well-known effects on neuronal activity, human sleep appears also to reorganize the infraslow (<0.1 Hz) oscillation hierarchy in brain. While wakefulness is dominated by unidirectional neurovascular coupling, in which neural activity predicts hemodynamic changes, our study shows that the change in brain state from wakefulness to sleep is accompanied by increased bidirectionality in prediction patterns. Sleep-related increases in signal power were associated with bidirectional prediction patterns involving electrical activity, vascular signals, and water volume changes. These multimodal findings highlight a fundamental change in coupling dependent on brain state, suggesting that both neural and nonneural alteration contribute to sleep-related brain function.
Web | DOI | PDF | Proceedings of the National Academy of Sciences | Open Access
