Increased temporolimbic cortical folding complexity in temporal lobe epilepsy

Abstract

Objective: Converging evidence suggests that abnormalities of brain development may play a role in the pathogenesis of temporal lobe epilepsy (TLE). As sulco-gyral patterns are thought to be a footprint of cortical development, we set out to quantitatively map folding complexity across the neocortex in TLE. Additionally, we tested whether there was a relationship between cortical complexity and features of hippocampal maldevelopment, commonly referred to as malrotation. Methods:To quantify folding complexity, we obtained whole-brain surface-based measures of absolute mean cortical curvature from MRI scans acquired in 43 drug-resistant patients with TLE with unilateral hippocampal atrophy, and 40 age-and sex-matched healthy controls. In patients, we correlated changes in cortical curvature with 3-dimensional measures of hippocampal positioning. Results:We found increased folding complexity in the temporolimbic cortices encompassing parahippocampal, temporopolar, insular, and fronto-opercular regions. Increased complexity was observed ipsilateral to the seizure focus in patients with left TLE (LTLE), whereas these changes were bilateral in patients with right TLE (RTLE). In both TLE groups, increased temporolimbic complexity was associated with increased hippocampal malrotation. We found tendencies for increased complexity in bilateral posterior temporal cortices in LTLE and contralateral parahippocampal cortices in RTLE to be predictive of unfavorable seizure outcome after surgery. Conclusion:The anatomic distribution of increased cortical complexity overlapping with limbic seizure networks in TLE and its association with hippocampal maldevelopment further imply that neurodevelopmental factors may play a role in the epileptogenic process of TLE. Neurology Growing evidence suggests abnormalities of brain development are etiologic factors contributing to the pathogenesis of temporal lobe epilepsy (TLE). Although hippocampal sclerosis is the histopathologic hallmark of this condition, detailed studies have shown concurrent abnormal dispersion of granule cells, remnant fetal Cajal-Retzius cells, and changes in architectural organization of CA1 and dentate gyrus indicative of underlying hippocampal developmental abnormalities.1 Additional data revealed increased temporal lobe white matter neuronal clustering 2 and abnormal cortical myelinated fibers resembling those found in malformations of cortical development.3,4 While current MRI techniques cannot readily identify these small-scale features, macroscopic markers of hippocampal maldevelopment (referred to as malrotation), identified as atypical shape and positioning, are found in 40% of patients with TLE. 5,6 The anatomic location and extent of potential cortical developmental anomalies in TLE remain largely unknown. Sulco-gyral patterns are thought to be a footprint of cortical developEditorial, page 117

Machine learning classification of mesial temporal sclerosis in epilepsy patients

“…Similar to previous studies on cortical thickness, the distribution of effects was relatively broad but had a predominance of effects in nearby frontal, temporal and limbic regions (Lin et al, 2007;Bernhardt et al, 2010;Kemmotsu et al, 2011). Additionally, measures of curvature and folding were found to be abnormal in ipsilateral temporal and frontal cortices, concordant with prior work (Voets et al, 2011;Alhusaini et al, 2012).…”

“…These findings are present in TLE patients with and without MTS but have been shown to be stronger in patients with MTS (Labate et al, 2011). Additionally, these methods allow for measurements of cortical folding and complexity, which have also been reported to be abnormal in individuals with TLE and MTS, particularly in ipsilateral temporal and frontal cortices (Voets et al, 2011;Alhusaini et al, 2012).…”

Autistic characteristics in adults with epilepsy

“…Previous evidence suggests that TLE may be the result of a neuro-developmental disorder (Voets et al, 2011). One explanation for these findings may be that those with TLE may have more uncontrolled epilepsy.…”

“…This suggests that maldevelopment in the cortex may lead to persistent changes in network properties within the brain, resulting in TLE. A recent study by Voets and colleagues (2011) explored the relationship of hippocampal malrotation, which is rarely found in individuals without seizures, and cortical abnormalities with TLE (Voets, Bernhardt, Kim, Yoon, & Bernasconi, 2011). The researchers found that TLE was associated with increased folding of the temporal limbic and neocortex, which the researchers' state is suggestive of a common neuro-developmental phenotype with maldevelopment of the temporal lobes, as an important factor in the development of TLE.…”

“…However, recent evidence suggests that the subtle cortical structure changes in TLE may indicate the existence of a common neuro-developmental phenotype (Voets et al, 2011). This suggests that for TLE alone, any significant findings may contribute to disentangle the neuro-developmental basis for ASD and epilepsy.…”