June Sic Kim

Thalamic changes in temporal lobe epilepsy with and without hippocampal sclerosis: A diffusion tensor imaging study

OBJECTIVE The seizure network may be different between temporal lobe epilepsy with hippocampal sclerosis (TLE+HS) and without HS (TLE-HS). Chronic seizure activity may alter the diffusion properties of a seizure network. The thalamus is known to have an anatomical connection to the medial temporal area and to play a role in seizure modulation. This study aimed to evaluate differences in thalamic changes between TLE+HS and TLE-HS with diffusion tensor imaging (DTI). METHODS Nine patients with TLE+HS and nine patients with TLE-HS were included in the study. All patients underwent surgery with good seizure outcomes. Hippocampal sclerosis was verified pathologically. Sixteen right-handed, normal subjects were enrolled as controls. DTI was acquired using 3.0 T MRI. The mean diffusivity (MD) and fractional anisotropy (FA) were calculated in the center of the bilateral thalamus with the DTIstudio program. RESULTS The MD of bilateral thalami increased in both TLE groups compared to controls (p<0.05), while FA values did not differ from controls. The MD of the thalamus ipsilateral to the epileptogenic side was higher in the TLE+HS group than in the TLE-HS group (p=0.007). Onset age, seizure duration, seizure frequency and total seizure number were not correlated with FA and MD changes (p>0.05). CONCLUSION Bilateral thalamic diffusion properties are altered in temporal lobe epilepsy. The presence of hippocampal sclerosis enhances the change ipsilaterally.

Blocking of irrelevant memories by posterior alpha activity boosts memory encoding

In our daily lives, we are confronted with a large amount of information. Because only a small fraction can be encoded in long‐term memory, the brain must rely on powerful mechanisms to filter out irrelevant information. To understand the neuronal mechanisms underlying the gating of information into long‐term memory, we employed a paradigm where the encoding was directed by a “Remember” or a “No‐Remember” cue. We found that posterior alpha activity increased prior to the “No‐Remember” stimuli, whereas it decreased prior to the “Remember” stimuli. The sources were localized in the parietal cortex included in the dorsal attention network. Subjects with a larger cue‐modulation of the alpha activity had better memory for the to‐be‐remembered items. Interestingly, alpha activity reflecting successful inhibition following the “No‐Remember” cue was observed in the frontal midline structures suggesting preparatory inhibition was mediated by anterior parts of the dorsal attention network. During the presentation of the memory items, there was more gamma activity for the “Remember” compared to the “No‐Remember” items in the same regions. Importantly, the anticipatory alpha power during cue predicted the gamma power during item. Our findings suggest that top‐down controlled alpha activity reflects attentional inhibition of sensory processing in the dorsal attention network, which then finally gates information to long‐term memory. This gating is achieved by inhibiting the processing of visual information reflected by neuronal synchronization in the gamma band. In conclusion, the functional architecture revealed by region‐specific changes in the alpha activity reflects attentional modulation which has consequences for long‐term memory encoding. Hum Brain Mapp 35:3972–3987, 2013.

Changes in Language Pathways in Patients with Temporal Lobe Epilepsy: Diffusion Tensor Imaging Analysis of the Uncinate and Arcuate Fasciculi

OBJECTIVE The language pathways consist of ventral and dorsal systems connected via the uncinate fasciculus and arcuate fasciculus, respectively. Seizures in medial temporal lobe epilepsy (mTLE) affect both tracts. Previous studies, however, have focused on the arcuate fasciculus to explain the language disturbance in mTLE. In contrast, we compared changes in both the uncinate and arcuate fasciculi using diffusion tensor imaging. METHODS Thirteen patients with left mTLE and 12 with right mTLE were studied. The Wada test showed left dominance for language in all these patients. Sixteen healthy right-handed subjects were also studied. The mean fractional anisotropy and mean apparent diffusion coefficient with their lateralization index of two fasciculi were compared between hemispheres and between subjects. RESULTS The mean apparent diffusion coefficient of the arcuate and uncinate fasciculi in both left- and right-mTLE patients increased bilaterally compared with that in healthy subjects. In left mTLE, the fractional anisotropy of the uncinate fasciculus was lower ipsilaterally (P = 0.002) and was significantly lateralized contralaterally (P < 0.001) compared with control subjects, whereas the fractional anisotropy of the arcuate fasciculus showed no lateralization (P = 0.577). In right mTLE, such a difference was not prominent. CONCLUSION The seizure network affects both arcuate and uncinate fasciculi bilaterally in both left- and right-mTLE patients. The change is most prominent in the left uncinate fasciculus in left mTLE.

Risk factor analysis of the development of new neurological deficits following supplementary motor area resection

OBJECT Supplementary motor area (SMA) resection often induces postoperative contralateral hemiparesis or speech disturbance. This study was performed to assess the neurological impairments that often follow SMA resection and to assess the risk factors associated with these postoperative deficits. METHODS The records for patients who had undergone SMA resection for pharmacologically intractable epilepsy between 1994 and 2010 were gleaned from an epilepsy surgery database and retrospectively reviewed in this study. RESULTS Forty-three patients with pharmacologically intractable epilepsy underwent SMA resection with intraoperative cortical stimulation and mapping while under awake anesthesia. The mean patient age was 31.7 years (range 15-63 years), and the mean duration and frequency of seizures were 10.4 years (range 0.1-30 years) and 14.6 per month (range 0.1-150 per month), respectively. Pathological examination of the brain revealed cortical dysplasia in 18 patients (41.9%), tumors in 16 patients (37.2%), and other lesions in 9 patients (20.9%). The mean duration of the follow-up period was 84.0 months (range 24-169 months). After SMA resection, 23 patients (53.5%) experienced neurological deficits. Three patients (7.0%) experienced permanent deficits, and 20 (46.5%) experienced symptoms that were transient. All permanent deficits involved contralateral weakness, whereas the transient symptoms patients experienced were varied, including contralateral weaknesses in 15, apraxia in 1, sensory disturbances in 1, and dysphasia in 6. Thirteen patients recovered completely within 1 month. Univariate analysis revealed that resection of the SMA proper, a shorter lifetime seizure history (<10 years), and resection of the cingulate gyrus in addition to the SMA were associated with the development of neurological deficits (p=0.078, 0.069, and 0.023, respectively). Cingulate gyrus resection was the only risk factor identified on multivariate analysis (p=0.027, OR 6.530, 95% CI 1.234-34.562). CONCLUSIONS Resection of the cingulate gyrus in addition to the SMA was significantly associated with the development of postoperative neurological impairment.

Resection frequency map after awake resective surgery for non-lesional neocortical epilepsy involving eloquent areas

BackgroundThe resection of eloquent areas is challenging due to postoperative neurological deficits. The purpose of this study was to assess the efficacy and risk of awake brain surgery for non-lesional epilepsy involving the eloquent areas or their adjacent areas and to advocate the generation of a resection frequency map.MethodsWe enrolled 55 patients who underwent awake surgery between 1994 and 2007 for non-lesional epilepsy involving the primary sensori-motor or language areas. All patients underwent two-staged operations including subdural electrode monitoring and awake resective surgery. For each case, the preoperative and postoperative images were spatially normalized and compared on a standard atlas, and the resection map was then computed by summing up each resected area on the atlas.ResultsThe postoperative seizure outcome was Engel class I in 27 patients (49.1%), II in nine (16.4%), III in 14 (25.5%) and IV in five (9.1%). Ten patients (18.2%) experienced postoperative neurological deficits including seven transient (12.7%) and three permanent, but mild ones (5.5%). The neurological complication rate of purely eloquent area resection was 36.8% (7/19). The resection frequency map computed in this study showed that the resection of eloquent areas was tolerable, with the exception of the Broca’s area.ConclusionsAwake resective surgery with intraoperative brain mapping is an effective and safe treatment option for non-lesional epilepsy involving eloquent areas. The resection frequency map can show the resected area of a group as well as individuals and provide an objective measure of neurological risk.

Formation of visual memories controlled by gamma power phase-locked to alpha oscillations.

Neuronal oscillations provide a window for understanding the brain dynamics that organize the flow of information from sensory to memory areas. While it has been suggested that gamma power reflects feedforward processing and alpha oscillations feedback control, it remains unknown how these oscillations dynamically interact. Magnetoencephalography (MEG) data was acquired from healthy subjects who were cued to either remember or not remember presented pictures. Our analysis revealed that in anticipation of a picture to be remembered, alpha power decreased while the cross-frequency coupling between gamma power and alpha phase increased. A measure of directionality between alpha phase and gamma power predicted individual ability to encode memory: stronger control of alpha phase over gamma power was associated with better memory. These findings demonstrate that encoding of visual information is reflected by a state determined by the interaction between alpha and gamma activity.

Functional Reorganization Associated with Semantic Language Processing in Temporal Lobe Epilepsy Patients after Anterior Temporal Lobectomy : A Longitudinal Functional Magnetic Resonance Image Study

OBJECTIVE The focus of this study is brain plasticity associated with semantic aspects of language function in patients with medial temporal lobe epilepsy (mTLE). METHODS Using longitudinal functional magnetic resonance imaging (fMRI), patterns of brain activation were observed in twelve left and seven right unilateral mTLE patients during a word-generation task relative to a pseudo-word reading task before and after anterior temporal section surgery. RESULTS No differences were observed in precentral activations in patients relative to normal controls (n = 12), and surgery did not alter the phonological-associated activations. The two mTLE patient groups showed left inferior prefrontal activations associated with semantic processing (word-generation > pseudo-word reading), as did control subjects. The amount of semantic-associated activation in the left inferior prefrontal region was negatively correlated with epilepsy duration in both patient groups. Following temporal resection, semantic-specific activations in inferior prefrontal region became more bilateral in left mTLE patients, but more left-lateralized in right mTLE patients. The longer the duration of epilepsy in the patients, the larger the increase in the left inferior prefrontal semantic-associated activation after surgery in both patient groups. Semantic activation of the intact hippocampus, which had been negatively correlated with seizure frequency, normalized after the epileptic side was removed. CONCLUSION These results indicate alternation of semantic language network related to recruitment of left inferior prefrontal cortex and functional recovery of the hippocampus contralateral to the epileptogenic side, suggesting an intra- and inter-hemispheric reorganization following surgery.

Magnetoencephalography Interictal Spike Clustering in Relation with Surgical Outcome of Cortical Dysplasia

Objective The aim of this study was to devise an objective clustering method for magnetoencephalography (MEG) interictal spike sources, and to identify the prognostic value of the new clustering method in adult epilepsy patients with cortical dysplasia (CD). Methods We retrospectively analyzed 25 adult patients with histologically proven CD, who underwent MEG examination and surgical resection for intractable epilepsy. The mean postoperative follow-up period was 3.1 years. A hierarchical clustering method was adopted for MEG interictal spike source clustering. Clustered sources were then tested for their prognostic value toward surgical outcome. Results Postoperative seizure outcome was Engel class I in 6 (24%), class II in 3 (12%), class III in 12 (48%), and class IV in 4 (16%) patients. With respect to MEG spike clustering, 12 of 25 (48%) patients showed 1 cluster, 2 (8%) showed 2 or more clusters within the same lobe, 10 (40%) showed 2 or more clusters in a different lobe, and 1 (4%) patient had only scattered spikes with no clustering. Patients who showed focal clustering achieved better surgical outcome than distributed cases (p=0.017). Conclusion This is the first study that introduces an objective method to classify the distribution of MEG interictal spike sources. By using a hierarchical clustering method, we found that the presence of focal clustered spikes predicts a better postoperative outcome in epilepsy patients with CD.

Localization of MEG pathologic gamma oscillations in adult epilepsy patients with focal cortical dysplasia

We aimed to evaluate the clinical value of gamma oscillations in MEG for intractable neocortical epilepsy patients with cortical dysplasia by comparing gamma and interictal spike events. A retrospective analysis of MEG recordings of 30 adult neocortical epilepsy patients was performed. Gamma (30–70 Hz) and interictal spike events were independently identified, their independent or concurrent presence determined, and their source localization rates compared. Of 30 patients, gamma activities were detected in 28 patients and interictal spikes in 24 patients. Gamma events alone appeared in 5 patients, interictal spikes alone in 1 patient, and no events in 1 patient. Gamma co-occurred with interictal spikes in 20.1 ± 22.1% and interictal spikes co-occurred with gamma in 15.0 ± 19.2%. Rates of event localization within the resection cavity were significantly different (p = 0.042) between gamma (63.3 ± 32.6%) and interictal spike (47.0 ± 41.3%) events. In 4 of the 5 gamma-only patients the mean localization rate was 42.5%. Compared with the interictal spike localization rate, 4 of 9 seizure-free patients had higher gamma localization rates, 4 had the same rate, and 1 had a lower rate. Individual gamma events can be detected independently from interictal spike presence. Gamma can be localized to the resection cavity at least comparably to or more frequently than that from interictal spikes. Even when interictal spikes were undetected, gamma sources were localized to the resection cavity. Gamma oscillations may be a useful indicator of epileptogenic focus.

Usefulness of interictal spike source localization in temporal lobe epilepsy: Electrocorticographic study

The success of epilepsy surgery depends on delineation of the suspected epileptogenic zone. The gold standard to delineate it is to use the ictal onset zone from an electrocorticography (ECoG). Although interictal spikes are also associated with the epileptogenic zone, their clinical significance has been under-evaluated. The aim of this study was to evaluate the source localization of interictal spikes in terms of the association with epileptogenic zone in surgical temporal lobe epilepsy patients. The proposition is that the resection volume in patients with favorable outcomes includes the epileptogenic zone. The association with the epileptogenic zone was assessed as follows: (1) how many of the interictal spike sources are within the resection volume in patients with favorable outcomes and (2) how many of the interictal spike sources are outside the resection volume in patients with unfavorable outcomes. Thirty-eight temporal lobe epilepsy (TLE) patients who underwent both ECoG monitoring and epilepsy surgery were recruited and their 10min of ECoG recordings were analyzed. Six tumor-related TLE patients were excluded in the analysis. Of the remaining 32 patients, 20 patients achieved favorable surgical outcomes (Engel I and II), while the surgical outcomes of 12 patients were unfavorable (Engel III and IV). In each patient, interictal spike sources were localized using sLORETA and co-registered into a reconstructed brain model. The correspondence rate with the resection volume was estimated by counting the percentage of interictal spike sources in the resection volume. The correspondence rate in patients with favorable outcomes was 72.8±22.1, which was significantly higher than that (41.2±28.8) of the patients with unfavorable outcomes (p=0.002). Nine out of twelve patients (75%) with unfavorable outcomes had multiple interictal spike source clusters both interior and exterior to the resection volume, while 4 of the 20 patients with favorable outcomes (20%) had such multiple clusters (p=0.021). In conclusion, interictal spike sources are highly associated with the epileptogenic zone. ECoG interictal spike source localization could help in the delineation of the potential resection volume.