Abstract
How epilepsy affects brain functional networks remains poorly understood. Here we investigated resting state functional connectivity of the temporal region in temporal lobe epilepsy. Thirty-two patients with unilateral temporal lobe epilepsy underwent resting state blood-oxygenation level dependent functional magnetic resonance imaging. We defined regions of interest a priori focusing on structures involved, either structurally or metabolically, in temporal lobe epilepsy. These structures were identified in each patient based on their individual anatomy. Our principal findings are decreased local and inter-hemispheric functional connectivity and increased intra-hemispheric functional connectivity ipsilateral to the seizure focus compared to normal controls. Specifically, several regions in the affected temporal lobe showed increased functional coupling with the ipsilateral insula and immediately neighboring subcortical regions. Additionally there was significantly decreased functional connectivity between regions in the affected temporal lobe and their contralateral homologous counterparts. Intriguingly, decreased local and inter-hemispheric connectivity was not limited or even maximal for the hippocampus or medial temporal region, which is the typical seizure onset region. Rather it also involved several regions in temporal neo-cortex, while also retaining specificity, with neighboring regions such as the amygdala remaining unaffected. These findings support a view of temporal lobe epilepsy as a disease of a complex functional network, with alterations that extend well beyond the seizure onset area, and the specificity of the observed connectivity changes suggests the possibility of a functional imaging biomarker for temporal lobe epilepsy.
Highlights
Focal epileptic seizures arise from focal abnormal neuronal activity which can spread to other cortical regions (Jackson and Colman, 1898)
Maccotta et al / NeuroImage: Clinical 2 (2013) 862–872 several brain regions becoming metabolically active during an epileptic seizure: in Temporal lobe epilepsy (TLE), for instance, the medial temporal region is not the only region active at seizure onset, but lateral temporal regions, the insula, the thalamus, and the contralateral temporal lobe are rapidly activated (Hogan et al, 2006). These findings suggest that focal epileptic seizures reflect abnormalities that go beyond the seizure onset zone and involve a network of regions, and that epilepsy reflects network-level instability or pathology (Spencer, 2002)
TLE appears to have a complex effect on the functional connectivity of mesial temporal and neocortical temporal regions
Summary
Focal epileptic seizures arise from focal abnormal neuronal activity which can spread to other cortical regions (Jackson and Colman, 1898). Temporal lobe epilepsy (TLE) is a well-characterized example of focal epilepsy, with seizures that typically originate in the medial temporal region. Localized structural and/or metabolic abnormalities extend beyond the medial temporal region to multiple, non-limbic brain regions, most prominently lateral temporal and frontal regions, as noted via structural magnetic resonance imaging (Bernhardt et al, 2010), positron emission tomography (Arnold et al, 1996; Theodore et al, 1992), magnetic resonance spectroscopy (Miller et al, 2000; Stanley et al, 1998), and pathologic studies (Margerison and Corsellis, 1966). Several patients have normal brain MRI or PET scans, even after years of disease (Carne et al, 2004; O'Brien et al, 1997; Siegel et al, 2001; Smith et al, 2011), suggesting that gross structural abnormalities alone incompletely capture the disease process
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