Structures involved at the time of temporal lobe spikes revealed by interindividual group analysis of EEG/fMRI data

Abstract

SUMMARYPurpose: We measured metabolic changes associated with temporal lobe (TL) spikes using combined electroencephalography (EEG) and functional magnetic resonance imaging (fMRI). We selected 18 patients with temporal lobe epilepsy (TLE) who underwent a 2-h simultaneous EEG-fMRI and had unilateral or bilateral independent TL spikes for interindividual group analysis, in order to identify consistent blood oxygenation level dependent (BOLD) responses to TL spikes. Methods: EEG was postprocessed and spikes were visually identified. fMRI data were preprocessed with motion correction, spatial smoothing, and removal of low frequency drifts. Spike timings were used as events for fMRI statistical analysis. Four hemodynamic response functions were used to account for variability in the BOLD response. Results: Group analysis revealed common areas of BOLD activations and deactivations. The hemodynamic response function (HRF) peaking 3 s after the spike showed activation involving ipsilaterally the mesial temporal structures (presumably the hippocampus), putamen/globus pallidus, inferior insula, and superior temporal gyrus. The HRF peaking at 5 s showed activations involving ipsiand contralaterally the superior temporal gyrus and inferior insula. Both HRFs showed bilateral posterior cingulate deactivations. Discussion: We disclosed involvement of a network of activated areas during unilateral TL spikes, including ipsilateral mesial temporal structures, basal ganglia, and bilateral neocortical temporal regions. Despite the low temporal resolution of fMRI we demonstrated that contralateral temporal involvement occurred later than ipsilateral activation. This contralateral change took place in the absence of visible EEG changes. The posterior cingulate deactivation may reflect the interconnections between this region and other limbic structures. It may also partially correspond to a suspension of the default mode network, as previously described for TL spikes.

Feasibility of an intracranial EEG–fMRI protocol at 3T: Risk assessment and image quality

“…Thus, time-consuming patient-specific optimization would be necessary with little potential benefit and reduced BOLD sensitivity in the rest of the brain away from the electrodes. This limitation is relevant since scalp EEG-fMRI studies have shown widespread BOLD signal changes suggestive of distributed epileptogenic networks underlying seemingly focal epileptiform discharges (Federico et al, 2005;Kobayashi et al, 2006Kobayashi et al, , 2009. Because previous studies support the superior BOLD sensitivity at 3 T compared to 1.5 T (Hoenig et al, 2005;Weiskopf et al, 2006), we believe that there would be a greater ability to detect BOLD signals at sites distant from the electrodes.…”

Do the basal ganglia inhibit seizure activity in temporal lobe epilepsy?

“…Largescale physiological brain network function seems to be impaired even in focal epilepsies [7,10,12]. Prominent connections between the striatum and mesiotemporal structures have been known for some time [40].…”

“…Magnetic resonance imaging, including functional magnetic resonance imaging (fMRI), fMRI-EEG, and spectroscopy [10][11][12][13][14] as well as PET and SPECT data [13][14][15][16][17][18][19] show that the BG play a role in various epileptic syndromes and various types of epileptic seizures.…”

The Default Mode Network and Altered Consciousness in Epilepsy

“…For example, neuroimaging studies in humans have shown decreased cerebral blood flow (CBF) in frontal and parietal cortex during these events [18,51,59] as well as with interictal discharges [39] causing deactivation in bilateral posterior cingulate during interictal spikes [37].…”