Intracranial EEG‐fMRI analysis of focal epileptiform discharges in humans

Abstract

SUMMARYPurpose: Combining intracranial electroencephalography (iEEG) with functional magnetic resonance imaging (fMRI) is of interest in epilepsy studies as it would allow the detection of much smaller interictal epileptiform discharges than can be recorded using scalp EEG-fMRI. This may help elucidate the spatiotemporal mechanisms underlying the generation of interictal discharges. To our knowledge, iEEG-fMRI has never been performed at 3 Tesla (3T) in humans. We report our findings relating to spike-associated blood oxygen level-dependent (BOLD) signal changes in two subjects. Methods: iEEG-fMRI at 3T was performed in two subjects. Twelve channels of iEEG were recorded from subdural strips implanted on the left posterior temporal and middle frontal lobes in a 20-year-old female with bilateral periventricular gray matter heterotopia. Twenty channels of iEEG were recorded bilaterally from two subdural strips laid anterior-posterior along mesial temporal surfaces in a 29-year-old woman with bilateral temporal seizures and mild left amygdalar enlargement on MRI. Functional MRI (fMRI) statistical maps were generated and thresholded at p = 0.01. Key Findings: No adverse events were noted. A total of 105 interictal discharges were recorded in the posterior middle temporal gyrus of Subject 1. In Subject 2, 478 discharges were recorded from both mesial temporal surfaces (n = 194 left, 284 right). The right and left discharges were modeled separately, as they were independent. Subject 1 showed spike-associated BOLD signal increases in the left superior temporal region, left middle frontal gyrus, and right parietal lobe. BOLD decreases were seen in the right frontal and parietal lobes. In Subject 2, BOLD signal increases were seen in both mesial temporal lobes, which when left and right spikes were modeled independently, were greater on the side of the discharge. In addition, striking BOLD signal decreases were observed in the thalamus and posterior cingulate gyrus. Significance: iEEG-fMRI can be performed at 3T with low risk. Notably, runs of only 5 or 10 min of EEG-fMRI were performed as part of our implementation protocol, yet a significant number of epileptiform discharges were recorded, allowing meaningful analyses. With these studies, we have shown that deactivation can be seen in individual subjects with focal epileptiform discharges. These preliminary observations suggest a novel mechanism through which focal interictal discharges may have widespread cortical and subcortical influences. KEY WORDS: Intracranial EEG, Functional MRI, EEGfMRI, Focal epilepsy.Electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) have been combined successfully to help localize changes in brain activity associated with interictal discharges (Cunningham et al., 2008;Gotman, 2008). Despite the success of scalp EEG-fMRI, scalp EEG has limited ability to detect discharges involving a small cortical area (<10 cm 2 ) or from deeper brain structures (Ebersole, 1997). The ability to detect low amplitude, deeply originat...

Connectomics and epilepsy

“…The whole-brain spatial detail of fMRI combined with the temporal resolution of EEG, which can capture the rapid cellular processes associated with epileptiform discharges, can be used to investigate the spatial extent of the epileptogenic network. Recent work has focused on developing well tolerated fMRI protocols in patients with intracranial electrodes that could provide depth EEG data and neurovascular function [22,23,24 ▪ ,25]. …”

Electrophysiological correlates of the BOLD signal for EEG-informed fMRI

“…In summary, a number of explanations for epilepsy‐related BOLD decreases have been offered, which may be explored further using simultaneous icEEG–fMRI data recorded in humans, with its exquisite local sensitivity [Cunningham et al, ; Vulliemoz et al, ].…”

Functional Magnetic Resonance Imaging Networks Induced by Intracranial Stimulation May Help Defining the Epileptogenic Zone

“…As we obtain results from more patients, these activation magnitudes could be compared with those derived from stimulation of normal tissue at the same location in an ensemble of prior patients. A second method for identification of the EZ would add spontaneous electroencephalographycorrelated fMRI (EEG-fMRI) (Cunningham et al, 2012;Gotman, 2008), whose patterns of activation represent a signature of the causative endogenous interictal discharges. If a stimulated DES-fMRI pattern can match the endogenous EEG-fMRI pattern, the location of active stimulation likely coincides with the location of the endogenous source.…”