Voxel‐based Optimized Morphometry (VBM) of Gray and White Matter in Temporal Lobe Epilepsy (TLE) with and without Mesial Temporal Sclerosis

Abstract

Summary:Purpose: In temporal lobe epilepsy (TLE) with evidence of hippocampal sclerosis (TLE-MTS) volumetric gray (GM) and white (WM) matter abnormalities are not restricted to the hippocampus but also are found in extrahippocampal structures. Less is known about extrahippocampal volumetric abnormalities in TLE without hippocampal sclerosis (TLE-no). In this study, we used optimized voxel-based morphometry (VBM) with and without modulation with the following aims: (a) to identify WM and GM abnormalities beyond the hippocampus in TLE-MTS and TLE-no; and (b) to determine whether extratemporal WM and GM abnormalities differ between TLE-MTS and TLEno.Methods: Optimized VBM of GM and WM with and without modulation was performed in 26 TLE-MTS (mean age, 35.6 ± 9.7 years), 17 TLE-no (mean age, 35.6 ± 11.1 years), and 30 healthy controls (mean age, 30.3 ± 11.1 years).Results: In TLE-MTS, GM/WM volume and concentration reductions were found in the ipsilateral limbic system, ipsi-and contralateral neocortical regions, thalamus, cerebellum, internal capsule, and brainstem when compared with controls. In contrast, no differences of GM/WM volumes/concentrations were found between TLE-no and controls or between TLE-no and TLE-MTS.Conclusions: In TLE-MTS, optimized VBM showed extensive GM and WM volume reductions in the ipsilateral hippocampus and in ipsi-and contralateral extrahippocampal regions. In contrast, no GM/WM volume or concentration reductions were found in TLE-no. This further supports the hypothesis that TLE-no is a distinct clinicopathologic entity from TLE-MTS and probably heterogeneous in itself. Key Words: TLE-Extratemporal-Voxel-based morphometryMesiotemporal sclerosis-Normal MRI.Mesial temporal lobe epilepsy (mTLE) is one of most frequent forms of partial epilepsy in adults. Based on neuroimaging and histologic characteristics, two main subtypes of mTLE can be distinguished: (a) TLE with hippocampal sclerosis (TLE-MTS), found in ∼60-70% of mTLE patients, which is characterized by an increased hippocampal T 2 signal and/or atrophied hippocampal formation on the MRI and significant neuronal loss in one or more hippocampal subfields in the histologic examination (1); and (b) MTLE without structural abnormalities on MRI (TLE-no) and only very mild or no neuronal loss in the hippocampus, which is found in ∼20-30% of mTLE patients. In both types of mTLE, seizures are not restricted to the medial temporal lobe but involve

Trajectories of brain remodeling in temporal lobe epilepsy

“…Our findings extend the reported findings on the effects of epilepsy on brain structure by demonstrating specific changes in MRI− patients. Conversely to published results showing either atrophy predominantly of the ipsilateral subiculum and CA1 [37] or absence of changes [16,32,38], we observe hippocampus volume increases in this TLE subgroup. The discrepant results could be interpreted as lack of statistical power in the previous studies or increased sensitivity of the applied computational methods for seizure-associated brain volume increases in the hippocampus [18].…”

Trajectories of brain remodeling in temporal lobe epilepsy

“…Our findings extend the reported findings on the effects of epilepsy on brain structure by demonstrating specific changes in MRI− patients. Conversely to published results showing either atrophy predominantly of the ipsilateral subiculum and CA1 [37] or absence of changes [16,32,38], we observe hippocampus volume increases in this TLE subgroup. The discrepant results could be interpreted as lack of statistical power in the previous studies or increased sensitivity of the applied computational methods for seizure-associated brain volume increases in the hippocampus [18].…”

Grey matter volume in healthy and epileptic beagles using voxel-based morphometry – a pilot study

“…The hippocampus of Beagles with IE had statistically significant reduced GMV that was even obvious, when all epileptic Beagles were calculated together. This finding is consistent with several human VBM studies about TLE [ 45 , 46 , 49 , 55 , 56 , 69 , 77 ]. Volumetric studies in veterinary medicine also showed hippocampal atrophy in epileptic dogs [ 24 , 44 ].…”

“…Our study also revealed a statistically significant loss of GMV in occipital gyrus in SE and epileptic Beagles. These findings are consistent with several human medicine studies of TLE patients [ 46 , 47 , 49 , 55 , 58 ].…”

Remodeling of brain morphology in temporal lobe epilepsy

“…The regions, decisive for TLE in absence of mesial temporal lobe pathology MRI−, represent a widespread distributed pattern including motor, premotor, and associative areas. Our findings corroborate previous reports demonstrating either absence of brain anatomy changes (Alhusaini et al., 2013; Coan, Campos, Beltramini, et al, 2014; Mueller et al., 2006; Peng et al., 2014) or implication of thalamus and sensorimotor cortex (Coan, Campos, Yasuda, et al, 2014; Labate et al., 2008; Mueller et al., 2009; Riederer et al., 2008). Preceding studies in MRI− TLE support the involvement of frontal and parietal cortices, especially the sensorimotor cortex mainly due to excitotoxicity induced neuronal loss (McDonald et al., 2008; Mueller et al., 2009).…”

Trajectories of brain remodeling in temporal lobe epilepsy

“…Our findings extend the reported findings on the effects of epilepsy on brain structure by demonstrating specific changes in MRI− patients. Conversely to published results showing either atrophy predominantly of the ipsilateral subiculum and CA1 [37] or absence of changes [16,32,38], we observe hippocampus volume increases in this TLE subgroup. The discrepant results could be interpreted as lack of statistical power in the previous studies or increased sensitivity of the applied computational methods for seizure-associated brain volume increases in the hippocampus [18].…”

Grey matter volume in healthy and epileptic beagles using voxel-based morphometry – a pilot study

“…The hippocampus of Beagles with IE had statistically significant reduced GMV that was even obvious, when all epileptic Beagles were calculated together. This finding is consistent with several human VBM studies about TLE [ 45 , 46 , 49 , 55 , 56 , 69 , 77 ]. Volumetric studies in veterinary medicine also showed hippocampal atrophy in epileptic dogs [ 24 , 44 ].…”

“…Our study also revealed a statistically significant loss of GMV in occipital gyrus in SE and epileptic Beagles. These findings are consistent with several human medicine studies of TLE patients [ 46 , 47 , 49 , 55 , 58 ].…”

Remodeling of brain morphology in temporal lobe epilepsy

“…The regions, decisive for TLE in absence of mesial temporal lobe pathology MRI−, represent a widespread distributed pattern including motor, premotor, and associative areas. Our findings corroborate previous reports demonstrating either absence of brain anatomy changes (Alhusaini et al., 2013; Coan, Campos, Beltramini, et al, 2014; Mueller et al., 2006; Peng et al., 2014) or implication of thalamus and sensorimotor cortex (Coan, Campos, Yasuda, et al, 2014; Labate et al., 2008; Mueller et al., 2009; Riederer et al., 2008). Preceding studies in MRI− TLE support the involvement of frontal and parietal cortices, especially the sensorimotor cortex mainly due to excitotoxicity induced neuronal loss (McDonald et al., 2008; Mueller et al., 2009).…”

Trajectories of brain remodeling in temporal lobe epilepsy

“…Our findings extend the reported findings on the effects of epilepsy on brain structure by demonstrating specific changes in MRI− patients. Conversely to published results showing either atrophy predominantly of the ipsilateral subiculum and CA1 [37] or absence of changes [16,32,38], we observe hippocampus volume increases in this TLE subgroup. The discrepant results could be interpreted as lack of statistical power in the previous studies or increased sensitivity of the applied computational methods for seizure-associated brain volume increases in the hippocampus [18].…”

Grey matter volume in healthy and epileptic beagles using voxel-based morphometry – a pilot study

“…The hippocampus of Beagles with IE had statistically significant reduced GMV that was even obvious, when all epileptic Beagles were calculated together. This finding is consistent with several human VBM studies about TLE [ 45 , 46 , 49 , 55 , 56 , 69 , 77 ]. Volumetric studies in veterinary medicine also showed hippocampal atrophy in epileptic dogs [ 24 , 44 ].…”

“…Our study also revealed a statistically significant loss of GMV in occipital gyrus in SE and epileptic Beagles. These findings are consistent with several human medicine studies of TLE patients [ 46 , 47 , 49 , 55 , 58 ].…”

Remodeling of brain morphology in temporal lobe epilepsy

“…The regions, decisive for TLE in absence of mesial temporal lobe pathology MRI−, represent a widespread distributed pattern including motor, premotor, and associative areas. Our findings corroborate previous reports demonstrating either absence of brain anatomy changes (Alhusaini et al., 2013; Coan, Campos, Beltramini, et al, 2014; Mueller et al., 2006; Peng et al., 2014) or implication of thalamus and sensorimotor cortex (Coan, Campos, Yasuda, et al, 2014; Labate et al., 2008; Mueller et al., 2009; Riederer et al., 2008). Preceding studies in MRI− TLE support the involvement of frontal and parietal cortices, especially the sensorimotor cortex mainly due to excitotoxicity induced neuronal loss (McDonald et al., 2008; Mueller et al., 2009).…”