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

Abstract

Purpose: 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 ipsi- and 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.

Figure 1

Group analysis results for the hemodynamic response function (HRF) peaking 3 s after the TL spikes. Resulting t-map (p < 0.005 noncorrected) after cluster size test (p < 0.05 corrected for spatial extent). (A) Sagittal slices (6 mm); (B) Coronal slices (6 mm). One cluster of significant blood oxygenation level dependent (BOLD) activation involved ipsilaterally the mesiotemporal structures (including the hippocampus), the putamen/globus pallidus, the inferior insula, and the superior temporal gyrus (cluster #1, Table 1). Significant BOLD deactivation was found in bilateral posterior cingulate regions (cluster #2, Table 1). Epilepsia © ILAE

Figure 2

Group analysis results for the hemodynamic response function (HRF) peaking 5 s after the temporal lobe (TL) spikes. Resulting t-map (p < 0.005 noncorrected) after cluster size test (p < 0.05 corrected for spatial extent). (A) Sagittal slices (6 mm); (B) Coronal slices (6 mm). Significant blood oxygenation level dependent (BOLD) activations were found ipsilaterally (cluster #3, Table 1) and contralaterally (cluster #4, Table 1) in the superior temporal gyrus and in the inferior insula. Significant BOLD deactivation was found in bilateral posterior cingulate regions (cluster #5, Table 1). Epilepsia © ILAE