University of Oulu

H. Helakari, J. Kananen, N. Huotari, L. Raitamaa, T. Tuovinen, V. Borchardt, A. Rasila, V. Raatikainen, T. Starck, T. Hautaniemi, T. Myllylä, O. Tervonen, S. Rytky, T. Keinänen, V. Korhonen, V. Kiviniemi, H. Ansakorpi, Spectral entropy indicates electrophysiological and hemodynamic changes in drug-resistant epilepsy – A multimodal MREG study, NeuroImage: Clinical, Volume 22, 2019, 101763, ISSN 2213-1582, https://doi.org/10.1016/j.nicl.2019.101763

Spectral entropy indicates electrophysiological and hemodynamic changes in drug-resistant epilepsy : a multimodal MREG study

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Author: Helakari, H.1,2,3; Kananen, J.1,2,3; Huotari, N.1,2,3;
Organizations: 1Oulu Functional NeuroImaging (OFNI), Department of Diagnostic Radiology, Oulu University Hospital, Oulu, Finland
2Medical Imaging, Physics and Technology (MIPT), The Faculty of Medicine, University of Oulu, Oulu, Finland
3Medical Research Center (MRC), Oulu, Finland
4Unit of Clinical Neurophysiology, Oulu University Hospital, Finland
5Biomedical Sensors in Translational Research, Optoelectronics and Measurement Techniques Unit, University of Oulu, Oulu, Finland
6Research Unit of Clinical Neuroscience, University of Oulu, Oulu, Finland
7Neurology Clinic, Oulu University Hospital, Oulu, Finland
Format: article
Version: published version
Access: open
Online Access: PDF Full Text (PDF, 1.7 MB)
Persistent link: http://urn.fi/urn:nbn:fi-fe202002216147
Language: English
Published: Elsevier, 2019
Publish Date: 2020-02-21
Description:

Abstract

Objective: Epilepsy causes measurable irregularity over a range of brain signal frequencies, as well as autonomic nervous system functions that modulate heart and respiratory rate variability. Imaging dynamic neuronal signals utilizing simultaneously acquired ultra-fast 10 Hz magnetic resonance encephalography (MREG), direct current electroencephalography (DC-EEG), and near-infrared spectroscopy (NIRS) can provide a more comprehensive picture of human brain function. Spectral entropy (SE) is a nonlinear method to summarize signal power irregularity over measured frequencies. SE was used as a joint measure to study whether spectral signal irregularity over a range of brain signal frequencies based on synchronous multimodal brain signals could provide new insights in the neural underpinnings of epileptiform activity.

Methods: Ten patients with focal drug-resistant epilepsy (DRE) and ten healthy controls (HC) were scanned with 10 Hz MREG sequence in combination with EEG, NIRS (measuring oxygenated, deoxygenated, and total hemoglobin: HbO, Hb, and HbT, respectively), and cardiorespiratory signals. After pre-processing, voxelwise SEMREG was estimated from MREG data. Different neurophysiological and physiological subfrequency band signals were further estimated from MREG, DC-EEG, and NIRS: fullband (0–5 Hz, FB), near FB (0.08–5 Hz, NFB), brain pulsations in very-low (0.009–0.08 Hz, VLFP), respiratory (0.12–0.4 Hz, RFP), and cardiac (0.7–1.6 Hz, CFP) frequency bands. Global dynamic fluctuations in MREG and NIRS were analyzed in windows of 2 min with 50% overlap.

Results: Right thalamus, cingulate gyrus, inferior frontal gyrus, and frontal pole showed significantly higher SEMREG in DRE patients compared to HC. In DRE patients, SE of cortical Hb was significantly reduced in FB (p = .045), NFB (p = .017), and CFP (p = .038), while both HbO and HbT were significantly reduced in RFP (p = .038, p = .045, respectively). Dynamic SE of HbT was reduced in DRE patients in RFP during minutes 2 to 6. Fitting to the frontal MREG and NIRS results, DRE patients showed a significant increase in SEEEG in FB in fronto-central and parieto-occipital regions, in VLFP in parieto-central region, accompanied with a significant decrease in RFP in frontal pole and parietal and occipital (O2, Oz) regions.

Conclusion: This is the first study to show altered spectral entropy from synchronous MREG, EEG, and NIRS in DRE patients. Higher SEMREG in DRE patients in anterior cingulate gyrus together with SEEEG and SENIRS results in 0.12–0.4 Hz can be linked to altered parasympathetic function and respiratory pulsations in the brain. Higher SEMREG in thalamus in DRE patients is connected to disturbances in anatomical and functional connections in epilepsy. Findings suggest that spectral irregularity of both electrophysiological and hemodynamic signals are altered in specific way depending on the physiological frequency range.

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Series: NeuroImage. Clinical
ISSN: 2213-1582
ISSN-E: 2213-1582
ISSN-L: 2213-1582
Volume: 22
Article number: UNSP 101763
DOI: 10.1016/j.nicl.2019.101763
OADOI: https://oadoi.org/10.1016/j.nicl.2019.101763
Type of Publication: A1 Journal article – refereed
Field of Science: 3126 Surgery, anesthesiology, intensive care, radiology
Subjects:
EEG
Funding: This work was supported by Health and Biosciences Doctoral programme -grant (HH), Jane and Aatos Erkko Foundation grant (VKi), Academy of Finland and Aivosäätiö TERVA grant 314497 (VKi,TM), Academy of Finland Grants 123772 & 275342 (VKi), The SalWe Research Program for Mind and Body (Tekes—the Finnish Funding Agency for Technology and Innovation, Grant No. 1104/10) (VKi), Novo Nordisk Foundation NNF17OC0030124 (TM), Finnish Medical Foundation (VKi, TT), Finnish Neurological Foundation, KEVO grants from Oulu University hospital (VKi), Epilepsy Research Foundation (JK), Finnish Cultural Foundation, North Ostrobothnia Regional Fund (JK), Orion Research Foundation sr (JK, TT), Tauno Tönning Foundation (JK).
Academy of Finland Grant Number: 314497
123772
Detailed Information: 314497 (Academy of Finland Funding decision)
123772 (Academy of Finland Funding decision)
Copyright information: © 2019 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license
  https://creativecommons.org/licenses/by-nc-nd/4.0/