Infra-slow fluctuations in cortical potentials and respiration drive fast cortical EEG rhythms in sleeping and waking states

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Journal Title

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Volume Title

A1 Alkuperäisartikkeli tieteellisessä aikakauslehdessä

Date

2023-12

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Mcode

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Language

en

Pages

13
207-219

Series

Clinical Neurophysiology, Volume 156

Abstract

Objective: Infra-slow fluctuations (ISF, 0.008–0.1 Hz) characterize hemodynamic and electric potential signals of human brain. ISFs correlate with the amplitude dynamics of fast (>1 Hz) neuronal oscillations, and may arise from permeability fluctuations of the blood–brain barrier (BBB). It is unclear if physiological rhythms like respiration drive or track fast cortical oscillations, and the role of sleep in this coupling is unknown. Methods: We used high-density full-band electroencephalography (EEG) in healthy human volunteers (N = 21) to measure concurrently the ISFs, respiratory pulsations, and fast neuronal oscillations during periods of wakefulness and sleep, and to assess the strength and direction of their phase-amplitude coupling. Results: The phases of ISFs and respiration were both coupled with the amplitude of fast neuronal oscillations, with stronger ISF coupling being evident during sleep. Phases of ISF and respiration drove the amplitude dynamics of fast oscillations in sleeping and waking states, with different contributions. Conclusions: ISFs in slow cortical potentials and respiration together significantly determine the dynamics of fast cortical oscillations. Significance: We propose that these slow physiological phases play a significant role in coordinating cortical excitability, which is a fundamental aspect of brain function.

Description

Funding Information: This work was funded by Jane & Aatos Erkko Foundation grants 1&210043 (V.Ki.), Academy of Finland Terva grants # 275342, 314497, 335720 (V.Ki), Aivosäätiö/BrainFoundation (J.K, V.Ki), Uniogs/MRC Oulu Doctoral Program-grant (H.H., J.K.), Pohjois-Suomen Terveydenhuollon tukisäätiö (H.H., V.Ko.), Instrumentarium Science Foundation (J.K), Emil Aaltonen Foundation (H.H, M.J), Finnish Medical Foundation (V.Ki., J.K., M.J.), VTR grants from Oulu University Hospital (V.Ki, V.Ko.), Finnish Neurological Foundation (V. Ki.), KEVO grants from Oulu University Hospital (V.Ki.), Orion Research Foundation (J.K.), Maire Taponen Foundation (J.K.). We acknowledge Inglewood Biomedical Editing for text revisions, Palva lab for providing a script for PTE calculation and CSC for computational resources. We thank Jussi Kantola for data management and Annastiina Kivipää for assistance during measurements and volunteer recruitment. Publisher Copyright: © 2023 International Federation of Clinical Neurophysiology

Keywords

Coupling, EEG, Modulation, Respiration, Sleep, Slow oscillation

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Citation

Väyrynen, T, Helakari, H, Korhonen, V, Tuunanen, J, Huotari, N, Piispala, J, Kallio, M, Raitamaa, L, Kananen, J, Järvelä, M, Palva, J M & Kiviniemi, V 2023, ' Infra-slow fluctuations in cortical potentials and respiration drive fast cortical EEG rhythms in sleeping and waking states ', Clinical Neurophysiology, vol. 156, pp. 207-219 . https://doi.org/10.1016/j.clinph.2023.10.013