Abstract

Objective: To evaluate local and distant blood oxygen level dependent (BOLD) signal changes related to interictal epileptiform discharges (IED) in drug-resistant temporal lobe epilepsy (TLE).Methods: Thirty-three TLE patients undergoing EEG–functional Magnetic Resonance Imaging (fMRI) as part of the presurgical workup were consecutively enrolled. First, a single-subject spike-related analysis was performed: (a) to verify the BOLD concordance with the presumed Epileptogenic Zone (EZ); and (b) to investigate the Intrinsic Connectivity Networks (ICN) involvement. Then, a group analysis was performed to search for common BOLD changes in TLE.Results: Interictal epileptiform discharges were recorded in 25 patients and in 19 (58%), a BOLD response was obtained at the single-subject level. In 42% of the cases, BOLD changes were observed in the temporal lobe, although only one patient had a pure concordant finding, with a single fMRI cluster overlapping (and limited to) the EZ identified by anatomo-electro-clinical correlations. In the remaining 58% of the cases, BOLD responses were localized outside the temporal lobe and the presumed EZ. In every patient, with a spike-related fMRI map, at least one ICN appeared to be involved. Four main ICNs were preferentially involved, namely, motor, visual, auditory/motor speech, and the default mode network. At the single-subject level, EEG–fMRI proved to have high specificity (above 65%) in detecting engagement of an ICN and the corresponding ictal/postictal symptom, and good positive predictive value (above 67%) in all networks except the visual one. Finally, in the group analysis of BOLD changes related to IED revealed common activations at the right precentral gyrus, supplementary motor area, and middle cingulate gyrus.Significance: Interictal temporal spikes affect several distant extra-temporal areas, and specifically the motor/premotor cortex. EEG–fMRI in patients with TLE eligible for surgery is recommended not for strictly localizing purposes rather it might be useful to investigate ICNs alterations at the single-subject level.

Highlights

  • Simultaneous EEG and fMRI (EEG–fMRI) recording is a functional neuroimaging technique that reveals cerebral hemodynamic changes related to interictal epileptiform discharges (IED) visualized on scalp EEG

  • The number of sessions recorded did not influence the average number of IEDs/run: patients with 1 session had a mean of 15 IEDs/run, patients with 2 sessions had a mean of 20.6 IEDs/run, patients with 3 sessions had a mean of 9.7 IEDs/run and the patient with 4 sessions recorded had a mean of 13.2 IEDs/run (p = 0.1073, two-tailed T-test between session 2 and session 3)

  • The group analysis including all patients (n = 25) revealed common BOLD changes related to IED at the right precentral gyrus, supplementary motor area (SMA), and middle cingulate gyrus

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Summary

Introduction

Simultaneous EEG and fMRI (EEG–fMRI) recording is a functional neuroimaging technique that reveals cerebral hemodynamic changes related to interictal epileptiform discharges (IED) visualized on scalp EEG. Modifications of BOLD signal related to temporal IED were observed in 50–83% of the patients in the different studies, and often, but notably in all cases, the fMRI response was localized in the temporal lobe, ipsilateral, or/and contralateral to the IED and in extra-temporal or subcortical structures. These findings are in line with the recent concept of “network epilepsy” applied to TLE, which has overcome the traditional hypothesis that in focal epilepsy seizure activity originates from a specific and anatomically isolated focus [12, 13]. The activity of the DMN, of attention, and of the executive control networks showed significant differences in patients with TLE when compared to healthy subjects

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