Temporal consistency of neurovascular components on awakening: preliminary evidence from electroencephalography, cerebrovascular reactivity, and functional magnetic resonance imaging

Ai Ling Hsu, Ming Kang Li, Yi Chia Kung, Zhitong John Wang, Hsin Chien Lee, Chia Wei Li, Chi Wen Cristina Huang*, Changwei W. Wu*

*Corresponding author for this work

Research output: Contribution to journalJournal Article peer-review

2 Scopus citations

Abstract

Sleep inertia (SI) is a time period during the transition from sleep to wakefulness wherein individuals perceive low vigilance with cognitive impairments; SI is generally identified by longer reaction times (RTs) in attention tasks immediately after awakening followed by a gradual RT reduction along with waking time. The sluggish recovery of vigilance in SI involves a dynamic process of brain functions, as evidenced in recent functional magnetic resonance imaging (fMRI) studies in within-network and between-network connectivity. However, these fMRI findings were generally based on the presumption of unchanged neurovascular coupling (NVC) before and after sleep, which remains an uncertain factor to be investigated. Therefore, we recruited 12 young participants to perform a psychomotor vigilance task (PVT) and a breath-hold task of cerebrovascular reactivity (CVR) before sleep and thrice after awakening (A1, A2, and A3, with 20 min intervals in between) using simultaneous electroencephalography (EEG)-fMRI recordings. If the NVC were to hold in SI, we hypothesized that time-varying consistencies could be found between the fMRI response and EEG beta power, but not in neuron-irrelevant CVR. Results showed that the reduced accuracy and increased RT in the PVT upon awakening was consistent with the temporal patterns of the PVT-induced fMRI responses (thalamus, insula, and primary motor cortex) and the EEG beta power (Pz and CP1). The neuron-irrelevant CVR did not show the same time-varying pattern among the brain regions associated with PVT. Our findings imply that the temporal dynamics of fMRI indices upon awakening are dominated by neural activities. This is the first study to explore the temporal consistencies of neurovascular components on awakening, and the discovery provides a neurophysiological basis for further neuroimaging studies regarding SI.

Original languageEnglish
Article number1058721
Pages (from-to)1058721
JournalFrontiers in Psychiatry
Volume14
DOIs
StatePublished - 2023

Bibliographical note

Copyright © 2023 Hsu, Li, Kung, Wang, Lee, Li, Huang and Wu.

Keywords

  • EEG power
  • cerebrovascular reactivity
  • neurovascular coupling
  • psychomotor vigilance task
  • simultaneous EEG-fMRI
  • sleep
  • sleep inertia

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