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Temporal lobe epilepsy is the most common form of focal epilepsy in adults, accounting for one third of all diagnosed epileptic patients, with seizures originating from or involving mesial temporal structures such as the hippocampus, and many of these patients being refractory to treatment with anti-epileptic drugs. Temporal lobe epilepsy is the most common childhood neurological disorder and, compared with adults, the symptoms are greatly affected by age and brain development. Diagnosis of temporal lobe epilepsy relies on clinical examination, patient history, electroencephalographic recordings, and brain imaging. Misdiagnosis or delay in diagnosis is common. A molecular biomarker that could distinguish epilepsy from healthy subjects and other neurological conditions would allow for an earlier and more accurate diagnosis and appropriate treatment to be initiated. Among possible biomarkers of pathological changes as well as potential therapeutic targets in the epileptic brain are microRNAs. Most of the recent studies had performed microRNA profiling in body fluids such as blood plasma and blood serum and brain tissues such as temporal cortex tissue and hippocampal tissue. A large number of microRNAs were dysregulated when compared to healthy controls and with some overlap between individual studies that could serve as potential biomarkers. For example, in adults with temporal lobe epilepsy, possible biomarkers are miR-199a-3p in blood plasma and miR-142-5p in blood plasma and blood serum. In adults with mesial temporal lobe epilepsy, possible biomarkers are miR-153 in blood plasma and miR-145-3p in blood serum. However, in many of the studies involving patients who receive one or several anti-epileptic drugs, the influence of these on microRNA expression in body fluids and brain tissues is largely unknown. Further studies are warranted with children with temporal lobe epilepsy and consideration should be given to utilizing mouse or rat and non-human primate models of temporal lobe epilepsy. The animal models could be used to confirm microRNA findings in human patients and to test the effects of targeting specific microRNAs on disease progression and behavior.
Temporal lobe epilepsy (TLE) is usually regarded as a polygenic and complex disorder. To understand its genetic component, numerous linkage analyses of familial forms and association studies of cases versus controls have been conducted since the middle of the nineties. The present paper lists genetic findings for TLE from the initial segregation analysis to the most recent results published in May 2011. To date, no genes have been clearly related to TLE despite many efforts to do so. However, it is vital to continue replication studies and collaborative attempts to find significant results and thus determine which gene variant combination plays a definitive role in the aetiology of TLE.
Mesial temporal lobe epilepsy (MTLE) is a network disorder. We aimed to quantify the white matter alterations in the temporal lobe of MTLE patients with hippocampal sclerosis (MTLE-HS) by using magnetic resonance fingerprinting (MRF), a novel imaging technique, which allows simultaneous measurements of multiple parameters with a single acquisition.
Temporal lobe epilepsy (TLE) is the most common form of adult epilepsy that is amenable to surgical treatment. In the carefully selected patient, excellent seizure outcome can be achieved with minimal or no side effects from surgery. This may result in improved psychosocial functioning, achieving higher education, and maintaining or gaining employment. The objective of this paper is to discuss the surgical selection process of a patient with TLE. We define what constitutes a patient that has medically refractory TLE, describe the typical history and physical examination, and distinguish between mesial TLE and neocortical TLE. We then review the role of routine (ambulatory/sleep-deprived electroencephalography (EEG), video EEG, magnetic resonance imaging (MRI), neuropsychological testing, and Wada testing) and ancillary preoperative testing (positron emission tomography, single-photon emission computed tomography (SPECT), subtraction ictal SPECT correlated to MRI (SISCOM), magnetoencephalography, magnetic resonance spectroscopy, and functional MRI) in selecting surgical candidates. We describe the surgical options for resective epilepsy surgery in TLE and its commonly associated risks while highlighting some of the controversies. Lastly, we present teaching cases to illustrate the presurgical workup of patients with medically refractory TLE.
In temporal lobe epilepsy (TLE), frontal-temporal connections are integral parts of the epileptogenic network. Although frontal-temporal gray matter abnormalities have been consistently demonstrated in TLE, white matter connections between these two lobes require further study in this disease setting. We therefore investigated the integrity of two major frontal-temporal white matter association tracts, uncinate fasciculus (UF) and arcuate fasciculus (AF), and their clinical correlates.
Doublecortin (DCX) is widely regarded as a marker of immature and migrating neurons during development. While DCX expression persists in adults, particularly in the temporal lobe and neurogenic regions, it is unknown how seizures influence its expression. The aim of the present study was to explore the distribution and characteristics of DCX-expressing cells in surgical and postmortem samples from 40 adult and paediatric patients, with epilepsy and with or without hippocampal sclerosis (HS), compared to post mortem controls. The hippocampus (pes and body), parahippocampal gyrus, amygdala, temporal pole and temporal cortex were examined with DCX immunohistochemistry using four commercially-available DCX antibodies, labelled cells were quantified in different regions of interest as well as their co-expression with cell type specific markers (CD68, Iba1, GFAP, GFAP∂, nestin, SOX2, CD34, OLIG2, PDGFRβ, NeuN) and cell cycle marker (MCM2). Histological findings were compared with clinical data, as well as gene expression data obtained from the temporal cortex of 83 temporal lobe epilepsy cases with HS. DCX immunohistochemistry identified immature (Nestin-/NeuN-) neurons in layer II of the temporal neocortex in patients with and without epilepsy. Their number declined significantly with age but was not associated with the presence of hippocampal sclerosis, seizure semiology or memory dysfunction. DCX+ cells were prominent in the paralaminar nuclei and periamygdalar cortex and these declined with age but were not significantly associated with epilepsy history. DCX expressing cells with ramified processes were prominent in all regions, particularly in the hippocampal subgranular zone, where significantly increased numbers were observed in epilepsy samples compared to controls. DCX ramified cells co-expressed Iba1, CD68 and PDGFRβ, and less frequently MCM2, OLIG2 and SOX2, but no co-localization was observed with CD34, nestin or GFAP/GFAP ∂. Gene expression data from neocortical samples in patients with TLE and HS supported ongoing DCX expression in adults. We conclude that DCX identifies a range of morphological cell types in temporal lobe epilepsy, including immature populations, glial and microglial cell types. Their clinical relevance and biological function requires further study but we show some evidence for alteration with age and in epilepsy.
To use proton Magnetic Resonance Spectroscopy (MRS) to measure in vivo temporal lobe GABA and glutamate plus glutamine (GLX) concentrations in patients with temporal lobe epilepsy (TLE) attributable to unilateral hippocampal sclerosis (HS) before and following anterior temporal lobe resection (ATLR).
Functional gradients have been used to study differences in connectivity between healthy and diseased brain states, however this work has largely focused on the cortex. Because the subcortex plays a key role in seizure initiation in temporal lobe epilepsy (TLE), subcortical functional-connectivity gradients may help further elucidate differences between healthy brains and TLE, as well as differences between left (L)-TLE and right (R)-TLE.
Functional magnetic resonance imaging (fMRI) in patients with temporal lobe epilepsy (TLE) has demonstrated reorganisation of language functions with greater involvement of the non-dominant hemisphere. The structural brain connections supporting this atypical language dominance have not previously been identified. We performed fMRI of language functions and imaging of white matter connections using MR tractography in 14 patients with unilateral TLE and hippocampal sclerosis and 10 controls. Verb generation and reading comprehension paradigms were used to define functional regions which were used to generate starting regions for tractography. Controls and right TLE patients had a left-lateralised pattern of both language-related activations and the associated structural connections. Left TLE patients showed more symmetrical language activations, along with reduced left hemisphere and increased right hemisphere structural connections. Subjects with more lateralised functional activation had also more highly lateralised connecting pathways. We provide evidence for structural reorganisation of white matter tracts that reflects the altered functional language lateralisation in left TLE patients. The combination of fMRI and tractography offers a promising tool for studying the reorganisation of language functions in many neurological conditions and may prove useful in predicting language deficits following temporal lobe surgery.
Many patients with mesial temporal lobe epilepsy continue to have seizures despite medical therapy. For these patients, one recourse is surgical resection of the mesial temporal lobe, with its attendant risks. Noninvasive treatment with Gamma Knife radiosurgery is under active investigation as a possible alternative to open surgery. Accumulated evidence from multiple studies shows radiosurgery to be comparable in outcomes to surgical resection. A definitive randomized, controlled trial, the Radiosurgery or Open Surgery for Epilepsy (ROSE) trial, is currently underway, and further investigation of this promising treatment is crucial in our advancement of alternative therapies to treat refractory epilepsy.
Recent in vitro and in vivo data show that acid-sensing ion channel 1a (ASIC1a) activation enhances neuronal excitability in the hippocampus and neocortex, indicating that ASIC1a might play a role in the generation and maintenance of epileptic seizures. The aim of this study was to investigate association of the ASIC1a gene with temporal lobe epilepsy (TLE) for the first time. Six tag single-nucleotide polymorphisms (SNPs) of the ASIC1a gene were selected and genotyped using polymerase chain reaction-restriction fragment length polymorphism in 560 TLE patients and 401 healthy controls. There was a significant allelic and genotypic association between rs844347:A>C and TLE compared with controls. The rs844347-A allele frequency was 88.1% in the patients and 83.0% in control subjects (OR=1.516, 95% CI 1.142-2.013, p=0.004). Furthermore, the haplotype analysis revealed a significant association with TLE. The results of this study demonstrate for the first time an association between an ASC1a variant allele and TLE in a Han Chinese population.
The correlation between clinical epilepsy and pathologic changes in the hippocampus was recognized in the early 1800s. However, the study of hippocampal pathology remained an anatomically descriptive discipline until the mid 1970s. In 1976, exploration of the electrical characteristics of the epileptic hippocampus and temporal neocortex began with the application of in vitro electrophysiologic techniques to human brain slices. Subsequently, recognition of the importance of neurotransmitters in epilepsy prompted ligand binding studies of receptor distributions in the epileptic brain. Recent refinements of DNA isolation and immunocytochemical techniques have led to the explosive development of antibodies to receptors, neurotransmitters, enzymes, and neurotransmitter transport systems. Since the 1980s, several alterations in epileptic hippocampus have been discovered with use of these pharmacologic and biochemical tools. The combination of anatomic, electrophysiologic, and biochemical experimental approaches has led to valuable insights into epilepsy-associated changes in temporal lobe tissue and has increased our understanding of the pathophysiology of temporal lobe epilepsy. Most of the summarized data in this review were derived from tissue excised from patients with medically intractable temporal lobe epilepsy or from postmortem brain. Although no attempt was made to cover the vast literature on animal models of epilepsy, some animal studies are discussed to illustrate current hypotheses that aid in the interpretation of the human findings.
Temporal lobe epilepsy, the most common type of epilepsy in adult humans, is characterized clinically by the progressive development of spontaneous recurrent seizures of temporal lobe origin and pathologically by hippocampal neuronal loss and mossy fiber sprouting. In this study, we sought to test the prominent hypothesis that neuronal loss and mossy fiber sprouting play a critical role in the genesis and progression of temporal lobe epilepsy. Rats receiving a single kainic acid injection experienced a single sustained episode of epileptic status with massive neuronal loss and mossy fiber sprouting, whereas rats receiving triple kainic acid injections experienced two priming episodes and one sustained episode of epileptic status with no detectable neuronal loss and mossy fiber sprouting. Early in the process of chronic seizure development, primed rats that failed to show detectable neuronal loss and mossy fiber sprouting exhibited a starting date and a frequency of spontaneous recurrent seizures similar to those of nonprimed rats that showed massive neuronal loss and mossy fiber sprouting. However, nonprimed rats displayed significantly prolonged episodes of spontaneous recurrent seizures over the whole process of chronic seizure development and more frequent severe seizures later in the process. Similar results were observed in both Fischer-344 and Wistar rats as well as in the rat pilocarpine preparation of temporal lobe epilepsy. These results fail to reveal a relation between neuronal loss-mossy fiber sprouting and the genesis of temporal lobe epilepsy but suggest that neuronal loss, mossy fiber sprouting, or both contribute to the intensification of chronic seizures.
Growing evidence of altered functional connectivity suggests that mesial temporal lobe epilepsy (mTLE) alters not only hippocampal networks, but also a number of resting state networks. These highly coherent, yet functionally distinct brain circuits interact dynamically with each other in order to mediate consciousness, memory, and attention. However, little is currently known about the modulation of these networks by epileptiform activity, such as interictal spikes and seizures. The objective of the study was to use simultaneous EEG-fMRI to investigate functional connectivity in three resting state networks: default mode network (DMN), salience network (SN), and dorsal attentional network (DAN) in patients with mTLE compared to a healthy cohort, and in relation to the onset of interictal spikes and the period immediately prior to the spikes. Compared to the healthy participants, mTLE patients showed significant alterations in functional connectivity of all three resting state networks, generally characterized by a lack of functional connectivity to prefrontal areas and increased connectivity to subcortical and posterior areas. Critically, prior to the onset of interictal spikes, compared to resting state, mTLE patients showed a lack of functional connectivity to the DMN and decreased synchronization within the SN and DAN, demonstrating alterations in functional coherence that may be responsible for the generation of epileptiform activity. Our findings demonstrate mTLE-related alterations of connectivity during the resting state as well as in relation to the onset of interictal spikes. These functional changes may underlie epilepsy-related cognitive abnormalities, because higher cognitive functions, such as memory or attention, rely heavily on the coordinated activity of all three resting state networks.
Although mesial temporal lobe epilepsy (mTLE) is characterized by the pathological changes in mesial temporal lobe, function alteration was also found in extratemporal regions. Our aim is to investigate the information flow between the epileptogenic zone (EZ) and other brain regions. Resting-state functional magnetic resonance imaging (RS-fMRI) data were recorded from 23 patients with left mTLE and matched controls. We first identified the potential EZ using the amplitude of low-frequency fluctuation (ALFF) of RS-fMRI signal, then performed voxel-wise Granger causality analysis between EZ and the whole brain. Relative to controls, patients demonstrated decreased driving effect from EZ to thalamus and basal ganglia, and increased feedback. Additionally, we found an altered causal relation between EZ and cortical networks (default mode network, limbic system, visual network and executive control network). The influence from EZ to right precuneus and brainstem negatively correlated with disease duration, whereas that from the right hippocampus, fusiform cortex, and lentiform nucleus to EZ showed positive correlation. These findings demonstrate widespread brain regions showing abnormal functional interaction with EZ. In addition, increased ALFF in EZ was positively correlated with the increased driving effect on EZ in patients, but not in controls. This finding suggests that the initiation of epileptic activity depends not only on EZ itself, but also on the activity emerging in large-scale macroscopic brain networks. Overall, this study suggests that the causal topological organization is disrupted in mTLE, providing valuable information to understand the pathophysiology of this disorder.
Functional gradients have been used to study differences in connectivity between healthy and diseased brain states, however this work has largely focused on the cortex. Because the subcortex plays a key role in seizure initiation in temporal lobe epilepsy (TLE), subcortical functional-connectivity gradients may help further elucidate differences between healthy brains and TLE, as well as differences between left (L)-TLE and right (R)-TLE.
Mesial temporal lobe epilepsy (TLE) is one of the most widespread neurological network disorders. Computational anatomy MRI studies demonstrate a robust pattern of cortical volume loss. Most statistical analyses provide information about localization of significant focal differences in a segregationist way. Multivariate Bayesian modeling provides a framework allowing inferences about inter-regional dependencies. We adopt this approach to answer following questions: Which structures within a pattern of dynamic epilepsy-associated brain anatomy reorganization best predict TLE pathology. Do these structures differ between TLE subtypes?
In those with drug refractory focal epilepsy, MR imaging is important for identifying structural causes of seizures that may be amenable to surgical treatment. In up to 25% of potential surgical candidates, however, MRI is reported as unremarkable even when employing epilepsy specific sequences. Automated MRI classification is a desirable tool to augment the interpretation of images, especially when changes are subtle or distributed and may be missed on visual inspection. Support vector machines (SVM) have recently been described to be useful for voxel-based MR image classification. In the present study we sought to evaluate whether this method is feasible in temporal lobe epilepsy, with adequate accuracy. We studied 38 patients with hippocampal sclerosis and unilateral (mesial) temporal lobe epilepsy (mTLE) (20 left) undergoing presurgical evaluation and 22 neurologically normal control subjects. 3D T1-weighted images were acquired at 3T (GE Excite), segmented into tissue classes, normalized and smoothed with SPM8. Diffusion tensor imaging (DTI) and double echo images for T2 relaxometry were also acquired and processed. The SVM analysis was done with the libsvm software package in a leave-one-out cross-validation design and predictive accuracy was measured. Local weighting was applied by SPM F-contrast maps. Best accuracies were achieved using the gray matter based segmentation (90-100%) and mean diffusivity (95-97%). For the three-way classification, accuracies were 88 and 93% respectively. Local weighting generally improved the accuracies except in the FA-based processing for which no effect was noted. Removing the hippocampus from the analysis, on the other hand, reduced the obtainable diagnostic indices but these were still >90% for DTI-based methods and lateralization based on gray matter maps. These findings show that automated SVM image classification can achieve high diagnostic accuracy in mTLE and that voxel-based MRI can be used at the individual subject level. This could be helpful for screening assessments of MRI scans in patients with epilepsy and when no lesion is detected on visual evaluation.
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