The neural tides of sleep and consciousness revealed by single-pulse electrical brain stimulation.
Kiyohide Usami, Anna Korzeniewska, Riki Matsumoto, Katsuya Kobayashi, Takefumi Hitomi, Masao Matsuhashi, Takeharu Kunieda, Nobuhiro Mikuni, Takayuki Kikuchi, Kazumichi Yoshida, Susumu Miyamoto, Ryosuke Takahashi, Akio Ikeda, Nathan E Crone
Sleep June 11, 2019 DOI: 10.1093/sleep/zsz050 (opens in new tab) via PubMed
Summary
AI-generated from the abstractThe sleep/wake cycle alters how neural activity spreads across large-scale brain networks. Using single-pulse electrical stimulation in patients with intracranial EEG electrodes, the study found that patterns of neural propagation at high-gamma frequencies (80-150 Hz) differ between wakefulness and sleep stages. During slow-wave sleep, frontal lobe stimulation produced greater propagation toward the parietal lobe than during wakefulness. During REM sleep, propagation decreased within the frontal lobe and increased within the parietal lobe. These directional biases in large-scale cortical network dynamics during REM sleep may help explain some unique experiential aspects of that sleep stage. The findings suggest that conscious awareness and sleep regulation involve changes in the balance of neural propagation across frontal-parietal networks.
Study at a glance
| Characteristics | Observational cohort Peer reviewed |
|---|---|
| Population | Patients implanted with intracranial EEG electrodes for epilepsy surgery |
| Intervention | single-pulse electrical stimulation |
| Keywords | Brain waves Causal interactions Effective connectivity High-gamma activity Human electrocorticography |
| Key finding | Patterns of neural propagation among cortical sites differ between wakefulness and different sleep stages, with frontal-to-parietal propagation increasing during slow-wave sleep and frontal propagation decreasing while parietal propagation increases during REM sleep. |
Abstract
Wakefulness and sleep arise from global changes in brain physiology that may also govern the flow of neural activity between cortical regions responsible for perceptual processing versus planning and action. To test whether and how the sleep/wake cycle affects the overall propagation of neural activity in large-scale brain networks, we applied single-pulse electrical stimulation (SPES) in patients implanted with intracranial EEG electrodes for epilepsy surgery. SPES elicited cortico-cortical spectral responses at high-gamma frequencies (CCSRHG, 80-150 Hz), which indexes changes in neuronal population firing rates. Using event-related causality (ERC) analysis, we found that the overall patterns of neural propagation among sites with CCSRHG were different during wakefulness and different sleep stages. For example, stimulation of frontal lobe elicited greater propagation toward parietal lobe during slow-wave sleep than during wakefulness. During REM sleep, we observed a decrease in propagation within frontal lobe, and an increase in propagation within parietal lobe, elicited by frontal and parietal stimulation, respectively. These biases in the directionality of large-scale cortical network dynamics during REM sleep could potentially account for some of the unique experiential aspects of this sleep stage. Together these findings suggest that the regulation of conscious awareness and sleep is associated with differences in the balance of neural propagation across large-scale frontal-parietal networks.