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

doi:10.3389/fpsyt.2023.1058721

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

Front Psychiatry. 2023 May 5:14:1058721. doi: 10.3389/fpsyt.2023.1058721. eCollection 2023.

Authors

Ai-Ling Hsu^{1

2}, Ming-Kang Li¹, Yi-Chia Kung³, Zhitong John Wang⁴, Hsin-Chien Lee^{5

6}, Chia-Wei Li⁷, Chi-Wen Cristina Huang⁷, Changwei W Wu^{4

8

8}

Affiliations

¹ Bachelor Program in Artificial Intelligence, Chang Gung University, Taoyuan, Taiwan.
² Department of Psychiatry, Chang Gung Memorial Hospital at Linkou, Taoyuan, Taiwan.
³ Department of Radiology, Tri-Service General Hospital, Taipei, Taiwan.
⁴ Graduate Institute of Mind, Brain and Consciousness, Taipei Medical University, Taipei, Taiwan.
⁵ Department of Psychiatry, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan.
⁶ Research Center of Sleep Medicine, Taipei Medical University Hospital, Taipei, Taiwan.
⁷ Department of Radiology, Wan Fang Hospital, Taipei Medical University, Taipei, Taiwan.
⁸ Brain and Consciousness Research Center, Taipei Medical University-Shuang Ho Hospital, New Taipei, Taiwan.

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.

Keywords: EEG power; cerebrovascular reactivity; neurovascular coupling; psychomotor vigilance task; simultaneous EEG-fMRI; sleep; sleep inertia.