Hemodynamic Response to Interictal Epileptiform Discharges Addressed by Personalized EEG-fNIRS Recordings

Giovanni Pellegrino, Alexis Machado, Nicolas von Ellenrieder, Satsuki Watanabe, Jeffery A. Hall, Jean-Marc Lina, Eliane Kobayashi, Christophe Grova

Objective: We aimed at studying the hemodynamic response (HR) to Interictal Epileptic Discharges (IEDs) using patient-specific and prolonged simultaneous ElectroEncephaloGraphy (EEG) and functional Near InfraRed Spectroscopy (fNIRS) recordings. Methods: The epileptic generator was localized using Magnetoencephalography source imaging. fNIRS montage was tailored for each patient, using an algorithm to optimize the sensitivity to the epileptic generator. Optodes were glued using collodion to achieve prolonged acquisition with high quality signal. fNIRS data analysis was handled with no a priori constraint on HR time course, averaging fNIRS signals to similar IEDs. Cluster-permutation analysis was performed on 3D reconstructed fNIRS data to identify significant spatio-temporal HR clusters. Standard (GLM with fixed HRF) and cluster-permutation EEG-fMRI analyses were performed for comparison purposes. Results: fNIRS detected HR to IEDs for 8/9 patients. It mainly consisted oxy-hemoglobin increases (seven patients), followed by oxy-hemoglobin decreases (six patients). HR was lateralized in six patients and lasted from 8.5 to 30 s. Standard EEG-fMRI analysis detected an HR in 4/9 patients (4/9 without enough IEDs, 1/9 unreliable result). The cluster-permutation EEG-fMRI analysis restricted to the region investigated by fNIRS showed additional strong and non-canonical BOLD responses starting earlier than the IEDs and lasting up to 30 s. Conclusions: (i) EEG-fNIRS is suitable to detect the HR to IEDs and can outperform EEG-fMRI because of prolonged recordings and greater chance to detect IEDs; (ii) cluster-permutation analysis unveils additional HR features underestimated when imposing a canonical HR function (iii) the HR is often bilateral and lasts up to 30 s.