Co-localization between the BOLD response and epileptiform discharges recorded by simultaneous intracranial EEG-fMRI at 3 T

Abstract

Objectives: Simultaneous scalp EEG-fMRI can identify hemodynamic changes associated with the generation of interictal epileptiform discharges (IEDs), and it has the potential of becoming a standard, non-invasive technique for pre-surgical assessment of patients with medically intractable epilepsy. This study was designed to assess the BOLD response to focal IEDs recorded via simultaneous intracranial EEG-functional MRI (iEEG-fMRI).

Methods: Twelve consecutive patients undergoing intracranial video EEG monitoring were recruited for iEEG-fMRI studies at 3 T. Depth, subdural strip, or grid electrodes were implanted according to our standard clinical protocol. Subjects underwent 10-60 min of continuous iEEG-fMRI scanning. IEDs were marked, and the most statistically significant clusters of BOLD signal were identified (Z-score 2.3, p value < 0.05). We assessed the concordance between the locations of the BOLD response and the IED. Concordance was defined as a distance <1.0 cm between the IED and BOLD response location. Negative BOLD responses were not studied in this project.

Results: Nine patients (7 females) with a mean age of 31 years (range 22-56) had 11 different types of IEDs during fMR scanning. The IEDs were divided based on the location of the active electrode contact into mesial temporal, lateral temporal, and extra-temporal. Seven (5 left) mesial temporal IED types were recorded in 5 patients (110-2092 IEDs per spike location). Six of these IEDs had concordant BOLD response in the ipsilateral mesial temporal structures, <1 cm from the most active contact. One of the two subjects with left lateral temporal IEDs had BOLD responses concordant with the location of the most active contact, as well other ipsilateral and contralateral sites. Notably, the remaining two subjects with extratemporal discharges showed no BOLD signal near the active electrode contact.

Conclusions: iEEG-fMRI is a feasible and low-risk method for assessment of hemodynamic changes of very focal IEDs that may not be recorded by scalp EEG. A high concordance rate between the location of the BOLD response and IEDs was seen for mesial temporal (6/7) IEDs. Significant BOLD activation was also seen in areas distant from the active electrode and these sites exhibited maximal BOLD activation in the majority of cases. This implies that iEEG-fMRI may further describe the areas involved in the generation of IEDs beyond the vicinity of the electrode(s).

Keywords: BOLD response; EEG-fMRI; Epileptiform discharge; IED, interictal epileptiform discharge; VEM, video-EEG monitoring.; intracranial EEG.

Fig. 1

Intracranial EEG recordings from patient 3. (A) Interictal iEEG recordings obtained in our Seizure Monitoring Unit. (B) Intracranial EEG of clinical quality acquired during simultaneous fMR image acquisition at 3 T. (C) Ictal iEEG recording of a right mesial temporal lobe seizure recorded in our Seizure Monitoring Unit. Note that the EEG samples in A and B are 1 s data segments containing interictal epileptiform discharges.

Fig. 2

Significant BOLD clusters associated with interictal discharges recorded via simultaneous iEEG-fMRI. (A) Mesial temporal lobe patients. Significant BOLD clusters (p < 0.05, AlphaSim correction) were found in all 5 subjects in this group. Two patients had independent, bilateral temporal discharges that were modeled independently of one another providing 7 datasets for analysis. A significant cluster is found adjacent to the active intracranial electrode contact (marked by a green circle) in 6/7 analyses. One patient (subject 5), had a large amount of susceptibility artifact in the left temporal lobe associated with a large amount of subject motion during data collection. (B) Lateral temporal lobe patients. Significant BOLD clusters (p < 0.05, AlphaSim correction) were found in both patients in this group. A significant cluster was found adjacent to the active intracranial electrode contact (green circle) in 1 of 2 analyses. (C) Extratemporal patients. Two patients with extra-temporal lobe epilepsy showed no significant clusters adjacent to the active electrode(s).