The dynamic functional connectivity peak index: Detection of interictal epileptic activity with fMRI

Objective Epileptogenic zone (EZ) localization is crucial for surgical treatment of patients with medication-resistant epilepsy. Although simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) can detect interictal discharges for EZ localization, clinical adoption is limited by the need for specialized equipment and expertise. Prior EEG-fMRI work has shown that interictal discharges produce fMRI activation in the EZ and deactivation in the default mode network. Here we use dynamic functional connectivity (dFC) to detect these opposing activations and localize potential interictal activity using fMRI without simultaneous EEG in a cohort composed primarily of temporal lobe epilepsy (TLE). Methods We quantified dFC with the edge timeseries approach and present examples of negative dynamic functional connectivity peaks following interictal discharges in two patients with TLE who received simultaneous EEG-fMRI. We defined the rate of these peaks as the "dFC peak index," hypothesizing it to be elevated in epileptic tissue. We assessed this hypothesis in 62 medication-resistant patients with focal epilepsy who underwent fMRI without simultaneous EEG (49 unilateral temporal, 11 bilateral temporal, 1 frontal, and 1 parietal). We Z-scored dFC peak index in each patient to healthy controls (n = 109) to identify regions with abnormally high values and tested whether these aligned with patients' EZs or correlated with clinical parameters. Results The dFC peak index was elevated in epileptic medial temporal structures in patients with TLE (pFWE <.05). Resection of regions with higher values correlated with better seizure outcomes after surgery (area under the curve [AUC] = .80, p = .0002), even in patients without hippocampal lesions on MRI (AUC = .79, p = .04). Significance This study presents the dFC peak index, which aims to detect interictal epileptic activity using fMRI without simultaneous EEG. Our results indicate that this measure is elevated in epileptic tissue in TLE, suggesting that it could provide unique information to guide epilepsy surgery.