Dynamic analysis on simultaneous iEEG-MEG data via hidden Markov model.


Journal

NeuroImage
ISSN: 1095-9572
Titre abrégé: Neuroimage
Pays: United States
ID NLM: 9215515

Informations de publication

Date de publication:
06 2021
Historique:
received: 14 07 2020
revised: 17 02 2021
accepted: 24 02 2021
pubmed: 5 3 2021
medline: 15 10 2021
entrez: 4 3 2021
Statut: ppublish

Résumé

Intracranial electroencephalography (iEEG) recordings are used for clinical evaluation prior to surgical resection of the focus of epileptic seizures and also provide a window into normal brain function. A major difficulty with interpreting iEEG results at the group level is inconsistent placement of electrodes between subjects making it difficult to select contacts that correspond to the same functional areas. Recent work using time delay embedded hidden Markov model (HMM) applied to magnetoencephalography (MEG) resting data revealed a distinct set of brain states with each state engaging a specific set of cortical regions. Here we use a rare group dataset with simultaneously acquired resting iEEG and MEG to test whether there is correspondence between HMM states and iEEG power changes that would allow classifying iEEG contacts into functional clusters. Simultaneous MEG-iEEG recordings were performed at rest on 11 patients with epilepsy whose intracranial electrodes were implanted for pre-surgical evaluation. Pre-processed MEG sensor data was projected to source space. Time delay embedded HMM was then applied to MEG time series. At the same time, iEEG time series were analyzed with time-frequency decomposition to obtain spectral power changes with time. To relate MEG and iEEG results, correlations were computed between HMM probability time courses of state activation and iEEG power time course from the mid contact pair for each electrode in equally spaced frequency bins and presented as correlation spectra for the respective states and iEEG channels. Association of iEEG electrodes with HMM states based on significant correlations was compared to that based on the distance to peaks in subject-specific state topographies. Five HMM states were inferred from MEG. Two of them corresponded to the left and the right temporal activations and had a spectral signature primarily in the theta/alpha frequency band. All the electrodes had significant correlations with at least one of the states (p < 0.05 uncorrected) and for 27/50 electrodes these survived within-subject FDR correction (q < 0.05). These correlations peaked in the theta/alpha band. There was a highly significant dependence between the association of states and electrodes based on functional correlations and that based on spatial proximity (p = 5.6e Epilepsy does not preclude HMM analysis of interictal data. The resulting group functional states are highly similar to those reported for healthy controls. Power changes recorded with iEEG correlate with HMM state time courses in the alpha-theta band and the presence of this correlation can be related to the spatial location of electrode contacts close to the individual peaks of the corresponding state topographies. Thus, the hypothesized relation between iEEG contacts and HMM states exists and HMM could be further explored as a method for identifying comparable iEEG channels across subjects for the purposes of group analysis.

Sections du résumé

BACKGROUND
Intracranial electroencephalography (iEEG) recordings are used for clinical evaluation prior to surgical resection of the focus of epileptic seizures and also provide a window into normal brain function. A major difficulty with interpreting iEEG results at the group level is inconsistent placement of electrodes between subjects making it difficult to select contacts that correspond to the same functional areas. Recent work using time delay embedded hidden Markov model (HMM) applied to magnetoencephalography (MEG) resting data revealed a distinct set of brain states with each state engaging a specific set of cortical regions. Here we use a rare group dataset with simultaneously acquired resting iEEG and MEG to test whether there is correspondence between HMM states and iEEG power changes that would allow classifying iEEG contacts into functional clusters.
METHODS
Simultaneous MEG-iEEG recordings were performed at rest on 11 patients with epilepsy whose intracranial electrodes were implanted for pre-surgical evaluation. Pre-processed MEG sensor data was projected to source space. Time delay embedded HMM was then applied to MEG time series. At the same time, iEEG time series were analyzed with time-frequency decomposition to obtain spectral power changes with time. To relate MEG and iEEG results, correlations were computed between HMM probability time courses of state activation and iEEG power time course from the mid contact pair for each electrode in equally spaced frequency bins and presented as correlation spectra for the respective states and iEEG channels. Association of iEEG electrodes with HMM states based on significant correlations was compared to that based on the distance to peaks in subject-specific state topographies.
RESULTS
Five HMM states were inferred from MEG. Two of them corresponded to the left and the right temporal activations and had a spectral signature primarily in the theta/alpha frequency band. All the electrodes had significant correlations with at least one of the states (p < 0.05 uncorrected) and for 27/50 electrodes these survived within-subject FDR correction (q < 0.05). These correlations peaked in the theta/alpha band. There was a highly significant dependence between the association of states and electrodes based on functional correlations and that based on spatial proximity (p = 5.6e
CONCLUSION
Epilepsy does not preclude HMM analysis of interictal data. The resulting group functional states are highly similar to those reported for healthy controls. Power changes recorded with iEEG correlate with HMM state time courses in the alpha-theta band and the presence of this correlation can be related to the spatial location of electrode contacts close to the individual peaks of the corresponding state topographies. Thus, the hypothesized relation between iEEG contacts and HMM states exists and HMM could be further explored as a method for identifying comparable iEEG channels across subjects for the purposes of group analysis.

Identifiants

pubmed: 33662572
pii: S1053-8119(21)00200-7
doi: 10.1016/j.neuroimage.2021.117923
pmc: PMC8204269
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

117923

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/L023784/2
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/K005464/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 203147/Z/16/Z
Pays : United Kingdom

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest None.

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Auteurs

Siqi Zhang (S)

Key Laboratory of Child Development and Learning Science of Ministry of Education, School of Biological Sciences & Medical Engineering, Southeast University, Nanjing 210096, Jiangsu, China; Wellcome Centre for Human Neuroimaging, UCL Institute of Neurology, 12 Queen Square, London WC1N 3BG, UK.

Chunyan Cao (C)

Department of Neurosurgery, affiliated Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.

Andrew Quinn (A)

Oxford Centre for Human Brain Activity, University of Oxford, Warneford Hospital, Oxford, UK.

Umesh Vivekananda (U)

Wellcome Centre for Human Neuroimaging, UCL Institute of Neurology, 12 Queen Square, London WC1N 3BG, UK; National Hospital for Neurology and Neurosurgery, Queen Square, London, UK.

Shikun Zhan (S)

Department of Neurosurgery, affiliated Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.

Wei Liu (W)

Department of Neurosurgery, affiliated Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.

Bomin Sun (B)

Department of Neurosurgery, affiliated Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.

Mark Woolrich (M)

Oxford Centre for Human Brain Activity, University of Oxford, Warneford Hospital, Oxford, UK.

Qing Lu (Q)

Key Laboratory of Child Development and Learning Science of Ministry of Education, School of Biological Sciences & Medical Engineering, Southeast University, Nanjing 210096, Jiangsu, China. Electronic address: luq@seu.edu.cn.

Vladimir Litvak (V)

Wellcome Centre for Human Neuroimaging, UCL Institute of Neurology, 12 Queen Square, London WC1N 3BG, UK. Electronic address: v.litvak@ucl.ac.uk.

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