Simultaneous Intracranial EEG-fMRI Shows Inter-Modality Correlation in Time-Resolved Connectivity Within Normal Areas but Not Within Epileptic Regions

Abstract

For the first time in research in humans, we used simultaneous icEEG-fMRI to examine the link between connectivity in haemodynamic signals during the resting-state (rs) and connectivity derived from electrophysiological activity in terms of the inter-modal connectivity correlation (IMCC). We quantified IMCC in nine patients with drug-resistant epilepsy (i) within brain networks in 'healthy' non-involved cortical zones (NIZ) and (ii) within brain networks involved in generating seizures and interictal spikes (IZ1) or solely spikes (IZ2). Functional connectivity (h ) estimates for 10 min of resting-state data were obtained between each pair of electrodes within each clinical zone for both icEEG and fMRI. A sliding window approach allowed us to quantify the variability over time of h (vh ) as an indicator of connectivity dynamics. We observe significant positive IMCC for h and vh , for multiple bands in the NIZ only, with the strongest effect in the lower icEEG frequencies. Similarly, intra-modal h and vh were found to be differently modified as a function of different epileptic processes: compared to NIZ, [Formula: see text] was higher in IZ1, but lower in IZ2, while [Formula: see text] showed the inverse pattern. This corroborates previous observations of inter-modal connectivity discrepancies in pathological cortices, while providing the first direct invasive and simultaneous comparison in humans. We also studied time-resolved FC variability multimodally for the first time, finding that IZ1 shows both elevated internal [Formula: see text] and less rich dynamical variability, suggesting that its chronic role in epileptogenesis may be linked to greater homogeneity in self-sustaining pathological oscillatory states.

Concurrent EEG- and fMRI-derived functional connectomes exhibit linked dynamics

“…Beyond the signal-to-noise limitations in human concurrent EEG-fMRI, there is evidence that γ-and β-band connectivity may contain information complementary to fMRI-derived connectivity. A weaker relation to fMRI connectivity has been reported for β and low-γ compared to other bands in intracranial electrophysiological recordings in humans (38,58) and in animals (59,60). The weaker relationship for β-and low γ-bands likely reflects a general property of the electrophysiology-fMRI relationship.…”

Interictal stereotactic-EEG functional connectivity in refractory focal epilepsies

“…Moreover, the same patients explored by stereotactic-EEG and functional MRI (at different times) exhibit increased functional connectivity in stereotactic-EEG but decreased functional connectivity using BOLD signals within epileptic structures (Bettus et al, 2011). A recent study confirmed this discrepancy in simultaneous recordings of functional MRI and stereotactic-EEG, demonstrating that intermodal connectivity correlation exists in non-epileptic structures but is altered in the epileptic zones (Ridley et al, 2017). Thus, whereas increased EEG connectivity could be related to pathologically reinforced links between hyperexcitable structures, decreased functional MRI connectivity could be more likely related to metabolic/perfusion alterations (Bettus et al, 2009).…”

“…Nevertheless, despite numerous studies on the subject, network organization in epilepsy remains incompletely understood (Richardson, 2012;Bernhardt et al, 2013;Duncan et al, 2016; Bartolomei et al, 2017). A large majority of literature has focused on MRI extracted connectivity (Bernhardt et al, 2013;Duncan et al, 2016) although the relationship between functional MRI and electrophysiological data is still incompletely understood (Bénar et al, 2006;Bettus et al, 2011;Coan et al, 2016;Ridley et al, 2017). Other studies used electrophysiological recordings (intracranial or not) to compute functional connectivity (Kramer et al, 2011;Chu et al, 2012;Kramer and Cash, 2012;van Diessen et al, 2013;Yaffe et al, 2015).…”

“…Stereotactic-EEG is a direct intracranial recording avoiding methodological issues in terms of source connectivity analysis, contrary to MEG or EEG that require an ill-posed inverse problem and are prone to source leakage (Schoffelen and Gross, 2009). Moreover, it is now clear that stereotactic-EEG and functional MRI data are not highly correlated (Bettus et al, 2011;Ridley et al, 2017). Despite the clear interest of stereotactic-EEG, stereotactic-EEG-extracted functional connectivity data from large cohorts of patients with extensive extra-temporal sampling remain scarce.…”

Brain regions and epileptogenicity influence epileptic interictal spike production and propagation during NREM sleep in comparison with wakefulness

“…Spikes were detected automatically with a spike detection algorithm (Amadeus software) during the selected parts of wakefulness and NREM sleep in each bipolar derivation. An experienced neurophysiologist then checked automatically detected spikes to corroborate them or not (Figure ).…”