Subdural Recordings Research Articles

A hybrid PDMS-Parylene subdural multi-electrode array

In this paper, we report on a cost effective and simple method for fabricating a flexible multi-electrode array for subdural neural recording. The electrode was fabricated using a PDMS-Parylene bilayer to combine the major advantages of both materials. Mechanical and electrical characterizations were performed to confirm functionality of a 16-site electrode array under various flexed/bent conditions. The electrode array was helically wound around a 3 mm diameter cylindrical tube and laid over a 2 cm diameter sphere while maintaining its recording capability. Experimental results showed impedance values between 300 kΩ and 600 kΩ at 1 kHz for 90 μm diameter gold recording sites. Acoustically evoked neural activity was successfully recorded from rat auditory cortex, confirming in vivo functionality.

Stereoelectroencephalography Following Subdural Grid Placement for Difficult to Localize Epilepsy

Despite the use of invasive subdural recording, failure to localize or resect the epileptogenic zone (EZ) occurs. Potential causes for this include EZ originating outside of the subdural grid coverage area, involvement of eloquent cortex, or complications requiring removal of electrodes without seizure localization. No study has examined the safety and efficacy of stereoelectroencephalography (SEEG) after subdural grid placement. To determine the efficacy of SEEG in patients who have previously undergone subdural grid placement. A prospective analysis was performed on 14 patients who had subdural grid evaluation and underwent subsequent SEEG monitoring. The follow-up period after the SEEG-guided resections ranged from 11 months to 34 months with an average follow-up of 20.1 months. Magnetic resonance imaging findings, EZ localization, outcomes, type of surgery, and perioperative complications were evaluated. Ten patients (71%) underwent a resection after SEEG reimplantation. Of the 4 patients (29%) not undergoing resection, 2 had seizures arising from eloquent cortex, 1 had bitemporal epilepsy, and 1 had a previous temporal lobectomy contralateral to the EZ. An estimate of the EZ was achieved in all patients based on interictal and ictal recordings. In patients undergoing resection, 60% were seizure-free at 11 months. Perioperative complications were minimal and included 1 abscess, which required burr-hole drainage and antibiotics. SEEG is a safe and effective method after subdural grid placement is inconclusive, providing an additional opportunity for seizure freedom in this highly challenging group of patients.

Stochastic Behavior of Phase Synchronization Index and Cross-Frequency Couplings in Epileptogenic Zones during Interictal Periods Measured with Scalp dEEG

The stochastic behavior of the phase synchronization index (SI) and cross-frequency couplings on different days during a hospital stay of three epileptic patients was studied for non-invasive localization of the epileptogenic areas from high density, 256-channel, scalp EEG (dEEG) recordings. The study was performed with short-duration (0–180 s), seizure-free, epileptiform-free, and spike-free interictal dEEG data on different days of three subjects. The seizure areas were localized with subdural recordings with an 8 × 8 macro-electrode grid array and strip electrodes. The study was performed in theta (3–7 Hz), alpha (7–12 Hz), beta (12–30 Hz), and low gamma (30–50 Hz) bands. A detrended fluctuation analysis was used to find the long range temporal correlations in the SI that reveals the stochastic behavior of the SI in a given time period. The phase synchronization was computed after taking Hilbert transform of the EEG data. Contour plots were constructed with 20 s time-frames using a montage of the layout of 256 electrode positions. It was found that the stochastic behavior of the SI was higher in epileptogenic areas and in nearby areas on different days for each subject. The low gamma band was found to be the best to localize the epileptic sites. Also, a stable higher pattern of SI emerged after 60–120 s in the epileptogenic areas. The cross-frequency couplings of SI in theta–gamma, beta–gamma, and alpha–gamma bands were decreased and spatial patterns were fragmented in epileptogenic areas. Combinations of an increase in the stochastic behavior of the SI and decrease in cross-frequency couplings are potential markers to assist in localizing epileptogenic areas. These findings suggest that it is possible to localize the epileptogenic areas non-invasively from a short-duration (∼180 s), seizure-free and spike-free interictal scalp dEEG recordings.

Ictal kissing with subdural EEG recording.

PurposeIctal kissing has been described in the literature. Five cases were reported and associated with temporal lobe epilepsy lateralizing to the nondominant hemisphere.MethodsA case of ictal kissing was identified. The aim was to demonstrate the clinical, clinical and electrophysiological features (as recorded by subdural electrodes). The surgical procedure, histopathology, and imaging data were reviewed and correlated with the literature.ResultsA 29-year-old right-handed female, who presented with ictal right hand left arm dystonic posturing, and lip smacking, was studied. The automatism was usually followed by prolonged emotional gestures and by hugging and kissing her relative and/or attendant nurse. Magnetic resonance imaging of the brain showed right small cortical and subcortical lesions of the right inferior frontal lobe with gliosis but without mass effect and normal-sized hippocampi. The PET scan showed hypometabolism of the right temporal lobe. Neuropsychological evaluation showed deficit in her nonverbal memory. The subdural electrodes showed high amplitude spikes over right mesial temporal lobe strips. The offsite of the ictal discharges was usually at the right frontal strips. Right standard temporal lobectomy with amygdalohippocampectomy and right inferior frontal lesionectomy were performed. The patient continued to be seizure-free for one year postoperatively.ConclusionOur case report supports with subdural EEG recording the findings of the few reported cases of ictal kissing behavior lateralized to the nondominant hemisphere. However, the affectionate kissing behavior was associated with spread of the epileptic discharges to the right frontal lobe.

Identifying the Epileptic Network

Identifying the Epileptic Network

Interictal PET and ictal subtraction SPECT: Sensitivity in the detection of seizure foci in patients with medically intractable epilepsy

Interictal positron emission tomography (PET) and ictal subtraction single photon emission computed tomography (SPECT) of the brain have been shown to be valuable tests in the presurgical evaluation of epilepsy. To determine the relative utility of these methods in the localization of seizure foci, we compared interictal PET and ictal subtraction SPECT to subdural and depth electrode recordings in patients with medically intractable epilepsy. Between 2003 and 2009, clinical information on all patients at our institution undergoing intracranial electroencephalography (EEG) monitoring was charted in a prospectively recorded database. Patients who underwent preoperative interictal PET and ictal subtraction SPECT were selected from this database. Patient characteristics and the findings on preoperative interictal PET and ictal subtraction SPECT were analyzed. Sensitivity of detection of seizure foci for each modality, as compared to intracranial EEG monitoring, was calculated. Fifty-three patients underwent intracranial EEG monitoring with preoperative interictal PET and ictal subtraction SPECT scans. The average patient age was 32.7 years (median 32 years, range 1-60 years). Twenty-seven patients had findings of reduced metabolism on interictal PET scan, whereas all 53 patients studied demonstrated a region of relative hyperperfusion on ictal subtraction SPECT suggestive of an epileptogenic zone. Intracranial EEG monitoring identified a single seizure focus in 45 patients, with 39 eventually undergoing resective surgery. Of the 45 patients in whom a seizure focus was localized, PET scan identified the same region in 25 cases (56% sensitivity) and SPECT in 39 cases (87% sensitivity). Intracranial EEG was concordant with at least one study in 41 cases (91%) and both studies in 23 cases (51%). In 16 (80%) of 20 cases where PET did not correlate with intracranial EEG, the SPECT study was concordant. Conversely, PET and intracranial EEG were concordant in two (33%) of the six cases where the SPECT did not demonstrate the seizure focus outlined by intracranial EEG. Thirty-three patients had surgical resection and >2 years of follow-up, and 21 of these (64%) had Engel class 1 outcome. No significant effect of imaging concordance on seizure outcome was seen. Interictal PET and ictal subtraction SPECT studies can provide important information in the preoperative evaluation of medically intractable epilepsy. Of the two studies, ictal subtraction SPECT appears to be the more sensitive. When both studies are used together, however, they can provide complementary information.

Increased Ictal Discharge Frequency and Neocortex Gliosis in Lateral Temporal Lobe Epilepsy

Medial temporal lobe epilepsy (TLE) with hippocampal sclerosis has both a scalp EEG initial ictal discharge frequency, which is faster, and also an intracranial EEG onset site that is more restricted to the hippocampus, than lateral TLE without hippocampal sclerosis. This study was performed to determine if lateral TLE patients have either intracranial EEG neocortical initial ictal frequencies or measures of lateral neocortex (LNC) histopathology that differ from patients whose seizures start in medial or multiple temporal lobe areas. Thirty-six TLE patients undergoing ictal depth and subdural strip electrode recordings were studied to determine the initial ictal discharge site (epileptogenic zone) within the temporal lobe and neocortical ictal frequency. In 25 patients, the number of reactive astrocytes in the neocortex and other measures of pathologic assessment of LNC were assessed. The initial neocortical ictal frequency was significantly faster when the initial ictal discharge was in the LNC ± medial paleocortex than either when it was in the hippocampus ± medial paleocortex or when it occurred simultaneously over the entire temporal lobe. Intracortical and Chaslin gliosis were both significantly greater when the initial ictal discharge was limited to the LNC than when it was in the hippocampus and/or medial paleocortex. Temporal lobe seizures originating in neocortex had a faster initial neocortical ictal frequency than seizures arising either medially in the hippocampus or widely over the whole temporal lobe. Epileptogenic zones limited to temporal neocortex were associated with greater intraneocortical and Chaslin gliosis compared with zones confined to medial structures.

Source reconstruction based on subdural EEG recordings adds to the presurgical evaluation in refractory frontal lobe epilepsy

ObjectiveIn presurgical investigations of refractory frontal lobe epilepsy, subdural EEG recordings offer extensive cortical coverage, but may overlook deep sources. Electrical Source Localization (ESL) from subdural recordings could overcome this sampling limitation. This study aims to assess the clinical relevance of this new method in refractory frontal lobe epilepsy associated with focal cortical dysplasia. MethodsIn 14 consecutive patients, we retrospectively compared: (i) the ESL of interictal spikes to the conventional irritative and seizure onset zones; (ii) the surgical outcome of cases with congruent ESL and resection volume to cases with incongruent ESL and resection volume. Each spike type was averaged to serve as a template for ESL by the MUSIC and sLORETA algorithms. Results were superimposed on the corresponding pre and post-surgical MRI. ResultsBoth ESL methods were congruent and consistent with conventional electroclinical analysis in all patients. In 7 cases, ESL identified a common deep source for spikes of different 2D localizations. The inclusion of ESL in the resection volume correlated with seizure freedom. ConclusionsESL from subdural recordings provided clinically relevant results in patients with refractory frontal lobe epilepsy. SignificanceESL complements the conventional analysis of subdural recordings. Its potential in improving tailored resections and surgical outcomes should be prospectively assessed.

Co-localizing linguistic and musical syntax with intracranial EEG

Despite general agreement on shared syntactic resources in music and language, the neuroanatomical underpinnings of this overlap remain largely unexplored. While previous studies mainly considered frontal areas as supramodal grammar processors, the domain-general syntactic role of temporal areas has been so far neglected. Here we capitalized on the excellent spatial and temporal resolution of subdural EEG recordings to co-localize low-level syntactic processes in music and language in the temporal lobe in a within-subject design. We used Brain Surface Current Density mapping to localize and compare neural generators of the early negativities evoked by violations of phrase structure grammar in both music and spoken language. The results show that the processing of syntactic violations relies in both domains on bilateral temporo-fronto-parietal neural networks. We found considerable overlap of these networks in the superior temporal lobe, but also differences in the hemispheric timing and relative weighting of their fronto-temporal constituents. While alluding to the dissimilarity in how shared neural resources may be configured depending on the musical or linguistic nature of the perceived stimulus, the combined data lend support for a co-localization of early musical and linguistic syntax processing in the temporal lobe.

Noninvasive Localization of Epileptic Sites from Stable Phase Synchronization Patterns on Different Days Derived from Short Duration Interictal Scalp dEEG

The stochastic behavior of the phase synchronization index (SI) on different days during a hospital stay of epileptic patients was studied for noninvasive localization of the epileptogenic areas from high density (256 channel) scalp EEG recordings. The study was performed on three subjects with interictal EEG data on different days. The seizure areas were localized with subdural recordings with an 8×8 grid electrode array. The study was performed in low gamma (30-50Hz) band with short duration (0-180s), seizure-free and spike-free scalp EEG data. A detrended fluctuation analysis was used to find the averaged stochastic fluctuations in the SI. The phase synchronization was computed after taking Hilbert transform of the EEG data. Contour plots were constructed with 20s time-frames using a montage of the layout of 256 electrode positions. It was found that the stochastic behavior of the SI was higher in epileptogenic areas on different days for each subject. Also, a stable higher pattern of SI emerged after 60-100s in the epileptogenic areas. These findings suggest that it is possible to localize the epileptogenic areas from the short duration (60-100s), seizure-free and spike-free high density scalp EEG recordings.

Automatic 80–250 Hz “ripple” high frequency oscillation detection in invasive subdural grid and strip recordings in epilepsy by a radial basis function neural network

ObjectiveRecent studies give evidence that high frequency oscillations (HFOs) in the range between 80Hz and 500Hz in invasive recordings of epilepsy patients have the potential to serve as reliable markers of epileptogenicity. This study presents an algorithm for automatic HFO detection. MethodsThe presented HFO detector uses a radial basis function neural network. Input features of the detector were energy, line length and instantaneous frequency. Visual marked “ripple” HFOs (80–250Hz) of 3 patients were used to train the neural network, and a further 8 patients served for the detector evaluation. ResultsDetector sensitivity and specificity were 49.1% and 36.3%. The linear and rank correlation between visual and automatic marked “ripple” HFO counts over the channels were significant for all recordings. A reference detector based on the line length achieved a sensitivity of 35.4% and a specificity of 46.8%. ConclusionsAutomatic detections corresponded only partly to visual markings for single events but the relative distribution of brain regions displaying “ripple” HFO activity is reflected by the automated system. SignificanceThe detector allows the automatic evaluation of brain areas with high HFO frequency, which is of high relevance for the demarcation of the epileptogenic zone.

The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes

Neuronal activity in the brain gives rise to transmembrane currents that can be measured in the extracellular medium. Although the major contributor of the extracellular signal is the synaptic transmembrane current, other sources--including Na(+) and Ca(2+) spikes, ionic fluxes through voltage- and ligand-gated channels, and intrinsic membrane oscillations--can substantially shape the extracellular field. High-density recordings of field activity in animals and subdural grid recordings in humans, combined with recently developed data processing tools and computational modelling, can provide insight into the cooperative behaviour of neurons, their average synaptic input and their spiking output, and can increase our understanding of how these processes contribute to the extracellular signal.

Imag(in)ing seizure propagation: MEG‐guided interpretation of epileptic activity from a deep source

Identification and accurate localization of seizure foci is vital in patients with medically-intractable focal epilepsy, who may be candidates for potentially curative resective epilepsy surgery. We present a patient with difficult-to-control seizures associated with an occult focal cortical dysplasia residing within the deeper left parietal operculum and underlying posterior insula, which was not detected by conventional MRI analysis. Propagated activities from this deeper generator produced misleading EEG patterns both on surface and subdural electrode recordings suggesting initial activation of the perirolandic and mesial frontal regions. However, careful spatio-temporal analysis of stereotyped interictal activities recorded during MEG, using sequential dipole modeling, revealed a consistent pattern of epileptic propagation originating from the deeper source and propagating within few milliseconds to the dorsal convexity. In this instance, careful dissection of noninvasive investigations (interictal MEG along with ictal SPECT findings) allowed clinicians to dismiss the inaccurate and misleading findings of the traditional "gold-standard" intracranial EEG. In fact, this multimodal noninvasive approach uncovered a subtle dysplastic lesion, resection of which rendered the patient seizure-free. This case highlights the potential benefits of dynamic analysis of interictal MEG in the appropriate clinical context. Pathways of interictal spike propagation may help elucidate essential neural networks underlying focal epilepsy.

Seizure Duration Determined by Subdural Electrode Recordings in Adult Patients with Intractable Focal Epilepsy

Background and Purpose:To investigate the duration of seizures and its relationship to seizure type, epilepsy syndrome, and seizure clustering.Methods:We examined 1,251 seizures from 152 patients who underwent video-electrocorticographic monitoring with subdural electrodes. Their seizure duration, seizure types, epilepsy syndromes, and seizure clusters were analyzed.Results:The median seizure duration was 91.5s (4–1016s). There were 34 (2.7%) seizures lasting > 5 minutes in 20 (13.2%) patients. There was a significant difference in seizure duration according to seizure types (p < 0.0001), but not to epilepsy syndromes. There were 99 seizure clusters in 67 (44.1%) patients. The first seizure in a cluster of seizures tended to last longer than non-cluster seizures (median 98s versus 89s, p = 0.033). Seizure duration was significantly longer in mesial temporal lobe epilepsy than in neocortical lobe epilepsy (median 103s versus 87s, p = 0.041). Rate of seizure cluster was lower in mTLE (38.0%) than in NLE (47.1%), but this difference was not significant.Conclusions:Seizure durations were different among seizure types. Seizure clustering also differ between patients with mTLE and those with NLE, which suggests different seizure generation and propagation among different epileptogenic foci. This study has implications for the identification of abnormally prolonged seizures.

Efficacy of temporal lobe surgery for epilepsy in patients with negative MRI for mesial temporal lobe sclerosis

Epilepsy surgery is a successful treatment for refractory temporal lobe epilepsy (TLE). Reports suggest fewer seizure-free outcomes for patients with TLE and who have a negative brain MRI (nMRI) for mesial temporal sclerosis. Data were collected prospectively from patients with nMRI who underwent temporal lobe surgery for TLE characterized by unilateral ictal temporal lobe seizure onset based on a scalp video electroencephalogram or invasive subdural electrode recordings. A total of 86 patients were followed for at least 24 months after surgery. Outcome was evaluated using the Engel classification. Seizure control was obtained by 55% (47/86) of patients (Class [CL]-I), 27% (23/86) showed significant improvement (CL-II) and 19% (16/86) were deemed surgical failures. Shorter duration of epilepsy, later onset of seizures, and ictal theta rhythm (5–7 Hz) were the most significant predictors of postoperative seizure control. Although hypometabolism on positron emission tomography scan and significant memory disparity (>2.5/8) were not significant prognosticators independently, cumulatively they were predictors for favorable outcome.

Spreading convulsions, spreading depolarization and epileptogenesis in human cerebral cortex

Spreading depolarization of cells in cerebral grey matter is characterized by massive ion translocation, neuronal swelling and large changes in direct current-coupled voltage recording. The near-complete sustained depolarization above the inactivation threshold for action potential generating channels initiates spreading depression of brain activity. In contrast, epileptic seizures show modest ion translocation and sustained depolarization below the inactivation threshold for action potential generating channels. Such modest sustained depolarization allows synchronous, highly frequent neuronal firing; ictal epileptic field potentials being its electrocorticographic and epileptic seizure its clinical correlate. Nevertheless, Leão in 1944 and Van Harreveld and Stamm in 1953 described in animals that silencing of brain activity induced by spreading depolarization changed during minimal electrical stimulations. Eventually, epileptic field potentials were recorded during the period that had originally seen spreading depression of activity. Such spreading convulsions are characterized by epileptic field potentials on the final shoulder of the large slow potential change of spreading depolarization. We here report on such spreading convulsions in monopolar subdural recordings in 2 of 25 consecutive aneurismal subarachnoid haemorrhage patients in vivo and neocortical slices from 12 patients with intractable temporal lobe epilepsy in vitro. The in vitro results suggest that γ-aminobutyric acid-mediated inhibition protects from spreading convulsions. Moreover, we describe arterial pulse artefacts mimicking epileptic field potentials in three patients with subarachnoid haemorrhage that ride on the slow potential peak. Twenty-one of the 25 subarachnoid haemorrhage patients (84%) had 656 spreading depolarizations in contrast to only three patients (12%) with 55 ictal epileptic events isolated from spreading depolarizations. Spreading depolarization frequency and depression periods per 24 h recording episodes showed an early and a delayed peak on Day 7. Patients surviving subarachnoid haemorrhage with poor outcome at 6 months showed significantly higher total and peak numbers of spreading depolarizations and significantly longer total and peak depression periods during the electrocorticographic monitoring than patients with good outcome. In a semi-structured telephone interview 3 years after the initial haemorrhage, 44% of the subarachnoid haemorrhage survivors had developed late post-haemorrhagic seizures requiring anti-convulsant medication. In those patients, peak spreading depolarization number had been significantly higher [15.1 (11.4–30.8) versus 7.0 (0.8–11.2) events per day, P = 0.045]. In summary, monopolar recordings here provided unequivocal evidence of spreading convulsions in patients. Hence, practically all major pathological cortical network events in animals have now been observed in people. Early spreading depolarizations may indicate a risk for late post-haemorrhagic seizures.

The Dorsal Hippocampal Commissure: When Functionality Matters

The Dorsal Hippocampal Commissure: When Functionality Matters

Noninvasive Epileptic Seizure Localization from Stochastic Behavior of Short Duration Interictal High Density Scalp EEG Data

The stochastic behavior of the phase synchronization index (SI) in different EEG bands was examined for noninvasive localization of the epileptogenic areas from the short duration (30-60s), seizure-free and spike-free high density (256 channel) scalp EEG data. We also examined the cross-frequency and cross-electrode coupling in different EEG bands. EEG data of four subjects was used. The seizure areas were localized with subdural recordings with an 8×8 grid electrode array. It was found that the stochastic behavior of the SI in low gamma band (30-50Hz) was higher in epileptogenic areas. The beta (12-30Hz) band also showed similar tendencies. The stochastic behavior in theta (3-7Hz) band was depressed in the seizure area while it was widespread in large areas over the scalp in the alpha (7-12Hz) band. The stochastic behavior of the cross-frequency and cross-electrode couplings in theta-gamma, alpha-gamma and beta-gamma bands were decreased in the seizure areas for all four subjects. These findings suggest that it is possible to localize the epileptogenic areas from the short duration seizure-free and spike-free high density scalp EEG data.

SLORETA allows reliable distributed source reconstruction based on subdural strip and grid recordings

Source localization based on invasive recordings by subdural strip and grid electrodes is a topic of increasing interest. This simulation study addresses the question, which factors are relevant for reliable source reconstruction based on sLORETA. MRI and electrode positions of a patient undergoing invasive presurgical epilepsy diagnostics were the basis of sLORETA simulations. A boundary element head model derived from the MRI was used for the simulation of electrical potentials and source reconstruction. Focal dipolar sources distributed on a regular three-dimensional lattice and spatiotemporal distributed patches served as input for simulation. In addition to the distance between original and reconstructed source maxima, the activation volume of the reconstruction and the correlation of time courses between the original and reconstructed sources were investigated. Simulations were supplemented by the localization of the patient's spike activity. For noise-free simulated data, sLORETA achieved results with zero localization error. Added noise diminished the percentage of reliable source localizations with a localization error ≤15 mm to 67.8%. Only for source positions close to the electrode contacts the activation volume correctly represented focal generators. Time-courses of original and reconstructed sources were significantly correlated. The case study results showed accurate localization. sLORETA is a distributed source model, which can be applied for reliable grid and strip based source localization. For distant source positions, overestimation of the extent of the generator has to be taken into account. sLORETA-based source reconstruction has the potential to improve the localization of distributed generators in presurgical epilepsy diagnostics and cognitive neuroscience.

Dipole source analyses of laser evoked potentials obtained from subdural grid recordings from primary somatic sensory cortex

The cortical potentials evoked by cutaneous application of a laser stimulus (laser evoked potentials, LEP) often include potentials in the primary somatic sensory cortex (S1), which may be located within the subdivisions of S1 including Brodmann areas 3A, 3B, 1, and 2. The precise location of the LEP generator may clarify the pattern of activation of human S1 by painful stimuli. We now test the hypothesis that the generators of the LEP are located in human Brodmann area 1 or 3A within S1. Local field potential (LFP) source analysis of the LEP was obtained from subdural grids over sensorimotor cortex in two patients undergoing epilepsy surgery. The relationship of LEP dipoles was compared with dipoles for somatic sensory potentials evoked by median nerve stimulation (SEP) and recorded in area 3B (see Baumgärtner U, Vogel H, Ohara S, Treede RD, Lenz FA. J Neurophysiol 104: 3029-3041, 2010). Both patients had an early radial dipole in S1. The LEP dipole was located medial, anterior, and deep to the SEP dipole, which suggests a nociceptive dipole in area 3A. One patient had a later tangential dipole with positivity posterior, which is opposite to the orientation of the SEP dipole in area 3B. The reversal of orientations between modalities is consistent with the cortical surface negative orientation resulting from superficial termination of thalamocortical neurons that receive inputs from the spinothalamic tract. Therefore, the present results suggest that the LEP may result in a radial dipole consistent with a generator in area 3A and a putative later tangential generator in area 3B.