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Indication of dynamic neurovascular coupling from inconsistency between EEG and fMRI indices across sleep–wake states

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Abstract

Neurovascular coupling (NVC), the transient regional hyperemia following the evoked neuronal responses, is the basis of blood oxygenation level-dependent techniques and is generally adopted across physiological conditions, including the intrinsic resting state. However, the possibility of neurovascular dissociations across physiological alterations is indicated in the literature. To examine the NVC stability across sleep–wake states, we used electroencephalography (EEG) as the index of neural activity and functional magnetic resonance imaging (fMRI) as the measure of cerebrovascular response. Eight healthy adults were recruited for simultaneous EEG-fMRI recordings in nocturnal sleep. We compared the cross-modality (EEG vs. fMRI) consistency of functional indices (spectral amplitude and functional connectivity) among five states of wakefulness and sleep (state effect). We also segregated the brain into three main partitions (anterior, middle and posterior) for spatial assessments (regional effect). Significant state effects were found on δ, α and fMRI indices and regional effects on the α and fMRI indices. However, the cross-state EEG changes in spectral amplitude and functional connectivity did not consistently match the changes in the fMRI indices across sleep–wake states. In spectral amplitude, the δ band peaked at the N3 stage for all brain regions, while the fMRI fluctuation amplitude peaked at the N2 stage in the central and posterior regions. In regional connectivity, the inter-hemispheric connectivity of the δ band peaked at the N3 stage for all regions, but the bilateral fMRI connectivity showed the state changes in the anterior and central regions. The cross-modality inconsistencies across sleep–wake states provided preliminary evidence that the neurovascular relationship may not change in a linear consistency during NREM sleep. Thus, caution shall be exercised when applying the NVC presumption to investigating sleep/wake transitions, even among healthy young adults.

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Abbreviations

NVC:

Neurovascular coupling

NREM sleep:

Non-rapid-eye-movement sleep

EEG:

Electroencephalography

fMRI:

Functional magnetic resonance imaging

BOLD:

Blood oxygenation level-dependent

ALFF:

Amplitude of low-frequency fluctuations

AASM:

American Academy of Sleep Medicine

CBF:

Cerebral blood flow

LFP:

Local field potential

AAL:

Automated Anatomical Labeling

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Acknowledgements

This research was funded by Taiwan Ministry of Science and Technology (MOST 104-2420-H-038-001-MY3, MOST 105-2628-B-038-013-MY3 and MOST 108-2321-B-038-005-MY2) and Taipei Medical University-Wanfang Hospital research program (107TMU-WFH-17).

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Authors and Affiliations

  1. Graduate Institute of Mind, Brain and Consciousness, Taipei Medical University, No. 250, Wu-Xing Street, Xinyi District, Taipei, 11031, Taiwan, ROC

    Changwei W. Wu & Timothy J. Lane

  2. Research Center of Brain and Consciousness, Shuang Ho Hospital, New Taipei, Taiwan

    Changwei W. Wu & Timothy J. Lane

  3. Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, Taipei, Taiwan

    Pei-Jung Tsai

  4. National Institute on Drug Abuse, National Institutes of Health, Baltimore, USA

    Pei-Jung Tsai

  5. Department of Medical Imaging and Radiological Sciences, Kaohsiung Medical University, Kaohsiung, Taiwan

    Sharon Chia-Ju Chen

  6. Department of Radiology, Wan Fang Hospital, Taipei Medical University, No.111, Sec. 3, Xinglong Rd., Wenshan Dist., Taipei, 11696, Taiwan

    Chia-Wei Li, Ai-Ling Hsu & Chia-Yuen Chen

  7. Institute of Biomedical Electronics and Bioinformatics, National Taiwan University, Taipei, Taiwan

    Hong-Yi Wu

  8. Department of Biomedical Sciences and Engineering, National Central University, Taoyuan, Taiwan

    Yu-Ting Ko & Pai-Chuan Hung

  9. Science Education Center, National Taiwan Normal University, Taipei, Taiwan

    Chun-Yen Chang

  10. Institute of Neuroscience, National Yang-Ming University, Taipei, Taiwan

    Ching-Po Lin

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  1. Changwei W. Wu
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Corresponding authors

Correspondence to Timothy J. Lane or Chia-Yuen Chen.

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Conflict of interest

Changwei W. Wu declares that he has no conflict of interest. Pei-Jung Tsai declares that she has no conflict of interest. Sharon Chia-Ju Chen declares that she has no conflict of interest. Chia-Wei Li declares that he has no conflict of interest. Ai-Ling Hsu declares that she has no conflict of interest. Hong-Yi Wu declares that she has no conflict of interest. Yu-Ting Ko declares that he has no conflict of interest. Pai-Chuan Hung declares that he has no conflict of interest. Chun-Yen Chang declares that he has no conflict of interest. Ching-Po Lin declares that he has no conflict of interest. Timothy J. Lane declares that he has no conflict of interest. Chen, Chia-Yuen declares that she has no conflict of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the Institutional Review Board of National Yang-Ming University and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

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Wu, C.W., Tsai, PJ., Chen, S.CJ. et al. Indication of dynamic neurovascular coupling from inconsistency between EEG and fMRI indices across sleep–wake states. Sleep Biol. Rhythms 17, 423–431 (2019). https://doi.org/10.1007/s41105-019-00232-1

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  • DOI: https://doi.org/10.1007/s41105-019-00232-1

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