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

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

doi:10.1016/j.nicl.2019.101763

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

Neuroimage Clin. 2019:22:101763. doi: 10.1016/j.nicl.2019.101763. Epub 2019 Mar 12.

Authors

H Helakari¹, J Kananen², N Huotari², L Raitamaa², T Tuovinen², V Borchardt², A Rasila², V Raatikainen³, T Starck³, T Hautaniemi², T Myllylä⁴, O Tervonen², S Rytky⁵, T Keinänen³, V Korhonen², V Kiviniemi², H Ansakorpi⁶

Affiliations

¹ Oulu Functional NeuroImaging (OFNI), Department of Diagnostic Radiology, Oulu University Hospital, Oulu, Finland; Medical Imaging, Physics and Technology (MIPT), The Faculty of Medicine, University of Oulu, Oulu, Finland; Medical Research Center (MRC), Oulu, Finland. Electronic address: heta.helakari@oulu.fi.
² Oulu Functional NeuroImaging (OFNI), Department of Diagnostic Radiology, Oulu University Hospital, Oulu, Finland; Medical Imaging, Physics and Technology (MIPT), The Faculty of Medicine, University of Oulu, Oulu, Finland; Medical Research Center (MRC), Oulu, Finland.
³ Oulu Functional NeuroImaging (OFNI), Department of Diagnostic Radiology, Oulu University Hospital, Oulu, Finland; Medical Imaging, Physics and Technology (MIPT), The Faculty of Medicine, University of Oulu, Oulu, Finland; Medical Research Center (MRC), Oulu, Finland; Unit of Clinical Neurophysiology, Oulu University Hospital, Finland.
⁴ Oulu Functional NeuroImaging (OFNI), Department of Diagnostic Radiology, Oulu University Hospital, Oulu, Finland; Medical Imaging, Physics and Technology (MIPT), The Faculty of Medicine, University of Oulu, Oulu, Finland; Biomedical Sensors in Translational Research, Optoelectronics and Measurement Techniques Unit, University of Oulu, Oulu, Finland.
⁵ Unit of Clinical Neurophysiology, Oulu University Hospital, Finland.
⁶ Research Unit of Clinical Neuroscience, University of Oulu, Oulu, Finland; Neurology Clinic, Oulu University Hospital, Oulu, Finland; Medical Research Center (MRC), Oulu, Finland.

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 SE_MREG 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 SE_MREG 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 SE_EEG 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 SE_MREG in DRE patients in anterior cingulate gyrus together with SE_EEG and SE_NIRS results in 0.12-0.4 Hz can be linked to altered parasympathetic function and respiratory pulsations in the brain. Higher SE_MREG 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.

Keywords: EEG; Epilepsy; Irregularity; NIRS; Parasympathetic; Ultra-fast fMRI.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Cerebrovascular Circulation / physiology*
Drug Resistant Epilepsy / diagnostic imaging
Drug Resistant Epilepsy / physiopathology*
Electroencephalography / methods
Entropy
Female
Hemodynamics / physiology*
Humans
Image Processing, Computer-Assisted / methods*
Magnetic Resonance Imaging / methods
Male
Middle Aged
Neuroimaging / methods*
Spectroscopy, Near-Infrared / methods
Young Adult