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

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
JournalSleep
Volume42
Issue number6
DOIs
StatePublished - Jun 11 2019

Fingerprint

Deep Brain Stimulation
Consciousness
Wakefulness
Sleep
Parietal Lobe
Sleep Stages
REM Sleep
Frontal Lobe
Electric Stimulation
Brain
Causality
Epilepsy
Electrodes
Population

Keywords

  • brain waves
  • causal interactions
  • effective connectivity
  • high-gamma activity
  • human electrocorticography

ASJC Scopus subject areas

  • Clinical Neurology
  • Physiology (medical)

Cite this

The neural tides of sleep and consciousness revealed by single-pulse electrical brain stimulation. / Usami, Kiyohide; Korzeniewska, Anna; Matsumoto, Riki; Kobayashi, Katsuya; Hitomi, Takefumi; Matsuhashi, Masao; Kunieda, Takeharu; Mikuni, Nobuhiro; Kikuchi, Takayuki; Yoshida, Kazumichi; Miyamoto, Susumu; Takahashi, Ryosuke; Ikeda, Akio; Crone, Nathan E.

In: Sleep, Vol. 42, No. 6, 11.06.2019.

Research output: Contribution to journalArticle

Usami, K, Korzeniewska, A, Matsumoto, R, Kobayashi, K, Hitomi, T, Matsuhashi, M, Kunieda, T, Mikuni, N, Kikuchi, T, Yoshida, K, Miyamoto, S, Takahashi, R, Ikeda, A & Crone, NE 2019, 'The neural tides of sleep and consciousness revealed by single-pulse electrical brain stimulation', Sleep, vol. 42, no. 6. https://doi.org/10.1093/sleep/zsz050
Usami, Kiyohide ; Korzeniewska, Anna ; Matsumoto, Riki ; Kobayashi, Katsuya ; Hitomi, Takefumi ; Matsuhashi, Masao ; Kunieda, Takeharu ; Mikuni, Nobuhiro ; Kikuchi, Takayuki ; Yoshida, Kazumichi ; Miyamoto, Susumu ; Takahashi, Ryosuke ; Ikeda, Akio ; Crone, Nathan E. / The neural tides of sleep and consciousness revealed by single-pulse electrical brain stimulation. In: Sleep. 2019 ; Vol. 42, No. 6.
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