Abstract

EEG-correlated fMRI analysis is widely used to detect regional BOLD fluctuations that are synchronized to interictal epileptic discharges, which can provide evidence for localizing the ictal onset zone. However, the typical, asymmetrical and mass-univariate approach cannot capture the inherent, higher order structure in the EEG data, nor multivariate relations in the fMRI data, and it is nontrivial to accurately handle varying neurovascular coupling over patients and brain regions. We aim to overcome these drawbacks in a data-driven manner by means of a novel structured matrix-tensor factorization: the single-subject EEG data (represented as a third-order spectrogram tensor) and fMRI data (represented as a spatiotemporal BOLD signal matrix) are jointly decomposed into a superposition of several sources, characterized by space-time-frequency profiles. In the shared temporal mode, Toeplitz-structured factors account for a spatially specific, neurovascular ‘bridge’ between the EEG and fMRI temporal fluctuations, capturing the hemodynamic response’s variability over brain regions. By analyzing interictal data from twelve patients, we show that the extracted source signatures provide a sensitive localization of the ictal onset zone (10/12). Moreover, complementary parts of the IOZ can be uncovered by inspecting those regions with the most deviant neurovascular coupling, as quantified by two entropy-like metrics of the hemodynamic response function waveforms (9/12). Hence, this multivariate, multimodal factorization provides two useful sets of EEG-fMRI biomarkers, which can assist the presurgical evaluation of epilepsy. We make all code required to perform the computations available at https://github.com/svaneynd/structured-cmtf.

Highlights

  • Refractory epilepsy is a neurological disorder suffered by 30% of approximately 50 million epilepsy patients worldwide (World Health Organization, 2019), in which seizures cannot adequately be controlled by anti-epileptic medication

  • We show 1) the thresholded pseudo t-maps of the IEDrelated source in the fMRI domain, both for significant activation as for significant deactivation; 2) maps highlighting the ROIs of high hemodynamic response function (HRF) entropy and extremity; 3) the temporal profile sr, spatial profile mr and spectral profile gr of each source in the EEG domain; 4) the HRF waveforms in the different ROIs, and the HRF basis functions at convergence of the algorithm

  • We show five axial slices of each map: in each case, we show two slices near the highest and lowest voxels of the ictal onset zone (IOZ) or significant regions of the fMRI spatial signature; if applicable, the middle slice is the cross-section with most overlap between IOZ and spatial signature, and the two remaining slices lie halfway between this slice and the extremal slices; otherwise all three bulk slices are chosen with equal spacing between the extremal slices

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Summary

Introduction

Refractory epilepsy is a neurological disorder suffered by 30% of approximately 50 million epilepsy patients worldwide (World Health Organization, 2019), in which seizures cannot adequately be controlled by anti-epileptic medication. In the preparation of treatment via resective surgery, interictal epileptic discharges (IEDs) can be localized in the brain with simultaneous EEG-fMRI, which provides a good surrogate for mapping the seizure onset zone (Lemieux et al, 2001; Thornton et al, 2010; van Houdt et al, 2013; Grouiller et al, 2011; Zijlmans et al, 2007; An et al, 2013; Khoo et al, 2017). Remedies for several of these issues are not yet widely applied, or are not yet available

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