Depth versus surface: A critical review of subdural and depth electrodes in intracranial electroencephalographic studies.

Intracranial electroencephalographic (IEEG) recording, using subdural electrodes (SDEs) and stereoelectroencephalography (SEEG), plays a pivotal role in localizing the epileptogenic zone (EZ). SDEs, employed for superficial cortical seizure foci localization, provide information on two-dimensional seizure onset and propagation. In contrast, SEEG, with its three-dimensional sampling, allows exploration of deep brain structures, sulcal folds, and bihemispheric networks. SEEG offers the advantages of fewer complications, better tolerability, and coverage of sulci. Although both modalities allow electrical stimulation, SDE mapping can tessellate cortical gyri, providing the opportunity for a tailored resection. With SEEG, both superficial gyri and deep sulci can be stimulated, and there is a lower risk of afterdischarges and stimulation-induced seizures. Most systematic reviews and meta-analyses have addressed the comparative effectiveness of SDEs and SEEG in localizing the EZ and achieving seizure freedom, although discrepancies persist in the literature. The combination of SDEs and SEEG could potentially overcome the limitations inherent to each technique individually, better delineating seizure foci. This review describes the strengths and limitations of SDE and SEEG recordings, highlighting their unique indications in seizure localization, as evidenced by recent publications. Addressing controversies in the perceived usefulness of the two techniques offers insights that can aid in selecting the most suitable IEEG in clinical practice.

Manifestation of Hippocampal Interictal Discharges on Clinical Scalp EEG Recordings.

PURPOSE: Epileptiform activity limited to deep sources such as the hippocampus currently lacks reliable scalp correlates. Recent studies, however, have found that a subset of hippocampal interictal discharges may be associated with visible scalp signals, suggesting that some types of hippocampal activity may be monitored noninvasively. The purpose of this study is to characterize the relationship between these scalp waveforms and the underlying intracranial activity. METHODS: Paired intracranial and scalp EEG recordings obtained from 16 patients were used to identify hippocampal interictal discharges. Discharges were grouped by waveform shape, and spike-triggered averages of the intracranial and scalp signals were calculated for each group. Cross-correlation of intracranial and scalp spike-triggered averages was used to determine their temporal relationship, and topographic maps of the scalp were generated for each group. RESULTS: Cross-correlation of intracranial and scalp correlates resulted in two classes of scalp waveforms-those with and without time delays from the associated hippocampal discharges. Scalp signals with no delay showed topographies with a broad field with higher amplitudes on the side ipsilateral to the discharges and a left-right flip in polarity-observations consistent with the volume conduction of a single unilateral deep source. In contrast, scalp correlates with time lags showed rotational dynamics, suggesting synaptic propagation mechanisms. CONCLUSIONS: The temporal relationship between the intracranial and scalp signals suggests that both volume conduction and synaptic propagation contribute to these scalp manifestations. Furthermore, the topographic evolution of these scalp waveforms may be used to distinguish spikes that are limited to the hippocampus from those that travel to or engage other brain areas.

Electrophysiological markers of memory consolidation in the human brain when memories are reactivated during sleep.

Human accomplishments depend on learning, and effective learning depends on consolidation. Consolidation is the process whereby new memories are gradually stored in an enduring way in the brain so that they can be available when needed. For factual or event knowledge, consolidation is thought to progress during sleep as well as during waking states and to be mediated by interactions between hippocampal and neocortical networks. However, consolidation is difficult to observe directly but rather is inferred through behavioral observations. Here, we investigated overnight memory change by measuring electrical activity in and near the hippocampus. Electroencephalographic (EEG) recordings were made in five patients from electrodes implanted to determine whether a surgical treatment could relieve their seizure disorders. One night, while each patient slept in a hospital monitoring room, we recorded electrophysiological responses to 10 to 20 specific sounds that were presented very quietly, to avoid arousal. Half of the sounds had been associated with objects and their precise spatial locations that patients learned before sleep. After sleep, we found systematic improvements in spatial recall, replicating prior results. We assume that when the sounds were presented during sleep, they reactivated and strengthened corresponding spatial memories. Notably, the sounds also elicited oscillatory intracranial EEG activity, including increases in theta, sigma, and gamma EEG bands. Gamma responses, in particular, were consistently associated with the degree of improvement in spatial memory exhibited after sleep. We thus conclude that this electrophysiological activity in the hippocampus and adjacent medial temporal cortex reflects sleep-based enhancement of memory storage.

Hippocampal spikes have heterogeneous scalp EEG correlates important for defining IEDs.

OBJECTIVE: To identify scalp EEG correlates of hippocampal spikes in patients with mesial temporal lobe epilepsy (mTLE). METHODS: We recorded scalp and intracranial EEG simultaneously in 20 consecutive surgical candidates with mTLE. Hippocampal spikes were identified from depth electrodes during the first hour of sleep on the first night of recording in the epilepsy monitoring unit, and their scalp EEG correlates were identified. RESULTS: Hippocampal spiking rates varied widely from 101 to 2187 (556 ± 672, mean ± SD) spikes per hour among the subjects. Of the 16,398 hippocampal spikes observed in this study, 492 (3.0%) of hippocampal spikes with extensive involvement of lateral temporal cortex were associated with scalp interictal epileptiform discharges (IEDs) including spikes and sharp waves; 198 (1.2%) of hippocampal spikes with limited involvement of lateral temporal cortex were associated with sharp transients or sharp slow waves, and 78 (0.05%)of hippocampal spikes with no lateral temporal involvement were associated with small sharp spikes (SSS). SSS were not correlated with independent temporal neocortical spikes. CONCLUSIONS: There are morphologically heterogeneous scalp EEG correlates of hippocampal spikes including SSS, sharp transients, sharp slow waves, spikes, and sharp waves. SSS correlate with hippocampal spikes and are likely an EEG marker for mTLE. These findings have important clinical implications for the diagnosis and localization of mTLE, and provide new perspectives on criteria for defining scalp IEDs.

Laser interstitial thermal therapy for NPRL3-related epilepsy with multiple seizure foci: A case report.

Introduction: NPRL3 gene mutations cause autosomal dominant familial focal epilepsy of variable foci (FFEVF) and is characterized by focal epilepsy arising from different brain regions including temporal, frontal, parietal and occipital lobes. About 50% of patients with NPRL3 related epilepsy are resistant to medical treatment. Method: We present a case of 27 years old man with NPRL3 related focal drug-resistant epilepsy. Stereotactic EEG showed two independent seizure foci, namely, left hippocampus and left orbitofrontal cortices. He underwent laser interstitial thermal therapy for ablating both foci in the same procedure that led to seizure cessation. Conclusion: laser interstitial thermal therapy can be an effective treatment for drug resistant NPRL3 related focal epilepsy with better tolerance and less morbidity as compared to open surgical resection, particularly in those with multiple seizure foci.

Surgical Outcomes and EEG Prognostic Factors After Stereotactic Laser Amygdalohippocampectomy for Mesial Temporal Lobe Epilepsy.

Objective: To assess the seizure outcomes of stereotactic laser amygdalohippocampectomy (SLAH) in consecutive patients with mesial temporal lobe epilepsy (mTLE) in a single center and identify scalp EEG and imaging factors in the presurgical evaluation that correlate with post-surgical seizure recurrence. Methods: We retrospectively reviewed the medical and EEG records of 30 patients with drug-resistant mTLE who underwent SLAH and had at least 1 year of follow-up. Surgical outcomes were classified using the Engel scale. Univariate hazard ratios were used to evaluate the risk factors associated with seizure recurrence after SLAH. Results: The overall Engel class I outcome after SLAH was 13/30 (43%), with a mean postoperative follow-up of 48.9 ± 17.6 months. Scalp EEG findings of interictal regional slow activity (IRSA) on the side of surgery (HR = 4.05, p = 0.005) and non-lateralizing or contra-lateralizing seizure onset (HR = 4.31, p = 0.006) were negatively correlated with postsurgical seizure freedom. Scalp EEG with either one of the above features strongly predicted seizure recurrence after surgery (HR = 7.13, p < 0.001) with 100% sensitivity and 71% specificity. Significance: Understanding the factors associated with good or poor surgical outcomes can help choose the best candidates for SLAH. Of the variables assessed, scalp EEG findings were the most clearly associated with seizure outcomes after SLAH.

Rapid development of seizures and PRES in a COVID-19 patient.

Neurological dysfunction has been noted in up to 36% of patients hospitalized with COVID-19, and a variety of mechanisms of neurological injury are possible. Here we report the rapid development of PRES and acute seizures in a patient with COVID-19 infection and sickle cell disease. The combination of COVID and sickle cell disease may raise the risk of PRES and could contribute to the higher mortality rate of COVID in patients with sickle cell disease.

Chasing language through the brain: Successive parallel networks.

OBJECTIVE: To describe the spatio-temporal dynamics and interactions during linguistic and memory tasks. METHODS: Event-related electrocorticographic (ECoG) spectral patterns obtained during cognitive tasks from 26 epilepsy patients (aged: 9-60 y) were analyzed in order to examine the spatio-temporal patterns of activation of cortical language areas. ECoGs (1024 Hz/channel) were recorded from 1567 subdural electrodes and 510 depth electrodes chronically implanted over or within the frontal, parietal, occipital and/or temporal lobes as part of their surgical work-up for intractable seizures. Six language/memory tasks were performed, which required responding verbally to auditory or visual word stimuli. Detailed analysis of electrode locations allowed combining results across patients. RESULTS: Transient increases in induced ECoG gamma power (70-100 Hz) were observed in response to hearing words (central superior temporal gyrus), reading text and naming pictures (occipital and fusiform cortex) and speaking (pre-central, post-central and sub-central cortex). CONCLUSIONS: Between these activations there was widespread spatial divergence followed by convergence of gamma activity that reliably identified cortical areas associated with task-specific processes. SIGNIFICANCE: The combined dataset supports the concept of functionally-specific locally parallel language networks that are widely distributed, partially interacting in succession to serve the cognitive and behavioral demands of the tasks.

The clinical significance of small sharp spikes: A retrospective study of 909 patients in epilepsy monitoring unit.

OBJECTIVES: To determine the incidence and clinical significance of small sharp spikes (SSS) in the patient population of the adult Epilepsy Monitoring Unit (EMU). METHODS: This is a retrospective study of EEG data and medical records from consecutive patients who underwent video-EEG recording in the adult EMU from March 2013 to February 2019. SSS, interictal epileptiform discharges (IEDs), and ictal patterns were identified. RESULTS: Of the 909 patients reviewed, SSS were observed in110 (12.1 %) patients. Epilepsy was present in 101 of the 110 (91.8 %) patients with SSS and in 441 of the 799 (55.2 %) patients without SSS. The incidence of epilepsy was significantly higher in patients with SSS than in those without SSS (OR = 9.1, 95 % CI: 4.5-18.3, P < 0.01). The sensitivity of SSS for epilepsy was 18.6 % and the specificity was 97.5 %. The incidence of SSS was strongly correlated with the frequency of IEDs (OR 1.89; 95 %CI: 1.60-2.24, P < 0.01). When both present, SSS and IEDs were co-lateralized in the same hemisphere. CONCLUSIONS: There is a statistically significant association between SSS and focal epilepsy. SSS have similar clinical implications to IEDs in the lateralization and localization of temporal lobe seizures. SSS can be an epileptiform EEG pattern for temporal lobe epilepsy.

RTTBD-like activity in association with hippocampal ictal discharges in patients with temporal lobe epilepsy.

To determine clinical and intracranial EEG correlates of rhythmic temporal theta bursts of drowsiness (RTTBD) and assess its clinical significance in patients with temporal lobe epilepsy (TLE). A retrospective review of simultaneous scalp and intracranial video-EEG recordings from 28 patients with TLE was evaluated for epilepsy surgery. Scalp RTTBD patterns were identified and their clinical and intracranial EEG correlates were then determined on video-EEG recording using depth and subdural electrodes. Thirty-one RTTBD patterns on scalp EEG were observed in six (21%) of the 28 patients. Five (16%) of the RTTBD patterns occurred during wakefulness and 26 (84%) occurred during drowsiness and light sleep. The mean duration of RTTBD was 10 seconds (range: 3-28 seconds). RTTDB consistently correlated with hippocampal ictal discharges and was time-locked to the hippocampal seizures in which the ictal discharges evolved into rhythmic theta frequency (4-7-Hz) range. Ictal automatisms were observed during five (16%) RTTBD patterns, while cognitive impairment was observed in four (13%) of the 31 RTTBD patterns. Our findings show that scalp EEG correlates of hippocampal ictal discharges can resemble RTTBD and may be associated with ictal symptoms and cognitive impairment, indicating that RTTBD may rarely be an ictal EEG pattern in patients with TLE.

Stereotactic laser anterior corpus callosotomy for Lennox-Gastaut syndrome.

OBJECTIVE: Corpus callosotomy is an effective palliative treatment for drug-resistant Lennox-Gastaut syndrome (LGS). Laser interstitial thermal therapy has been increasingly used in the treatment of epilepsy. Here, we assess the safety and effectiveness of minimally invasive stereotactic laser anterior corpus callosotomy (SLACC) for drop attacks in LGS. METHODS: We reviewed sequential cases of patients with medically intractable LGS who underwent SLACC using a two-cannula technique between November 2014 and July 2019. Pre- and postoperative magnetic resonance imaging was used to measure the anteroposterior length of callosal ablation (contrast-enhancing lesion) and estimated disconnection (gap in tract projections on diffusion tensor imaging). Patients were followed longitudinally to assess clinical outcomes. RESULTS: Ten patients were included in this study. The median age was 33 (range = 11-52) years, median duration of epilepsy was 26 (range = 10-49) years, and median duration of postoperative follow-up was 19 (range = 6-40) months. In the anteroposterior direction, 53 ± 7% (mean ± SD) of the corpus callosum was ablated and 62 ± 19% of the corpus callosum was estimated to be disconnected. Six (60%) of 10 patients achieved >80% seizure reduction, two (20%) of whom became seizure-free. Eight (80%) patients had >80% reduction in drop attacks, five (50%) of whom became free of drop attacks. Three patients subsequently underwent laser posterior callosotomy with further improvement in drop attacks and/or overall seizure frequency. One patient had an asymptomatic intracerebral hemorrhage along the cannula tract. One patient developed significant aggression after becoming seizure-free. SIGNIFICANCE: Seizure outcomes following SLACC were comparable to previously reported outcomes of open callosotomy, with reasonable safety profile. SLACC appears to be an effective alternative to open anterior corpus callosotomy with minimal postoperative discomfort and a short recovery period.

Stereotactic laser interstitial thermal therapy for epilepsy associated with solitary and multiple cerebral cavernous malformations.

OBJECTIVE: The authors sought to perform a preliminary assessment of the safety and effectiveness of stereotactic laser interstitial thermal therapy (LITT) for patients with cerebral cavernous malformation (CCM)-related epilepsy. METHODS: The authors retrospectively analyzed 6 patients with CCM-related epilepsy who underwent LITT. Pre-, intra-, and postoperative brain MRI studies were used to characterize preoperative CCM volume, ablation volume, and postablation hemosiderin volume. Clinical outcomes were assessed postoperatively during clinic follow-up visits or phone interviews. RESULTS: LITT was performed in 7 CCMs in 6 patients. Two patients had familial CCM disease with multifocal lesions. Four treated CCMs were extratemporal, and 3 were in or near the visual pathways. The median follow-up was 25 (range 12-39) months. Five of 6 (83%) patients achieved seizure freedom (Engel I classification), of whom 4 (67%) were Engel IA and 1 was Engel IC after a single seizure on postoperative day 4. The remaining patient had rare seizures (Engel II). One patient had a nondisabling visual field deficit. There were no hemorrhagic complications. All patients were discharged within 24 hours postablation. MRI 3-11 months after ablation demonstrated expected focal necrosis and trace hemosiderin-related T2 hypointensity measuring 9%-44% (median 24%) of the original lesion volume, with significant (p = 0.04) volume reduction. CONCLUSIONS: LITT is a minimally invasive option for treating CCM-related epilepsy with seizure outcomes comparable to those achieved with open lesionectomy. The precision of LITT allows for the obliteration of eloquent, deep, small, and multifocal lesions with low complication rates, minimal postoperative discomfort, and short hospital stays. In this study the feasibility and benefits of this method were demonstrated in 2 patients with multifocal lesions.

DC shifts, high frequency oscillations, ripples and fast ripples in relation to the seizure onset zone.

Efforts to improve epilepsy surgery outcomes have led to increased interest in the study of electroencephalographic oscillations outside the conventional EEG bands. These include fast activity above the gamma band, known as high frequency oscillations (HFOs), and infraslow activity (ISA) below the delta band, sometimes referred to as direct current (DC) or ictal baseline shifts (IBS). HFOs in particular have been extensively studied as potential biomarkers for epileptogenic tissue in light of evidence showing that resection of brain tissue containing HFOs is associated with good surgical outcomes. Not all HFOs are conclusively pathological, however, as they can be recorded in nonepileptic tissue and induced by cognitive, visual, or motor tasks. Consequently, efforts to distinguish between pathological and physiological HFOs have identified several traits specific to pathological HFOs, such as coupling with interictal spikes, association with delta waves, and stereotypical morphologies. On the opposite end of the EEG spectrum, sub-delta oscillations have been shown to co-localize with the seizure onset zones (SOZ) and appear in a narrower spatial distribution than activity in the conventional EEG frequency bands. In this report, we review studies that implicate HFOs and ISA in ictogenesis and discuss current limitations such as inter-observer variability and poor standardization of recording techniques. Furthermore, we propose that HFOs and ISA should be analyzed in addition to activity in the conventional EEG band during intracranial presurgical EEG monitoring to identify the best possible surgical margin.

Clinical implications of scalp ictal EEG pattern in patients with temporal lobe epilepsy.

OBJECTIVE: To determine the clinical implications of scalp ictal EEG pattern in patients with temporal lobe epilepsy (TLE). METHODS: Scalp EEG ictal patterns were retrospectively determined in 27 consecutive patients with medically refractory temporal lobe epilepsy who underwent phase-1 scalp video-EEG and phase-2 simultaneous scalp and intracranial video-EEG recordings for pre-surgical evaluation. RESULTS: Of the 192 temporal lobe seizures recorded during phase-1 and phase-2 scalp video-EEG studies, 124 (65%) seizures were associated with theta/alpha (5-9 Hz) ictal onset pattern, and 68 (35%) seizures were associated with delta (2-5 Hz) ictal onset pattern. Fourteen (52%) patients had exclusively theta/alpha ictal onset, 3 (11%) patients had exclusively delta ictal onset, and 10 (37%) patients had mixed theta/alpha and delta ictal onsets. MTLE was observed in 26 patients who had 124 seizures with theta/alpha ictal onset and 59 seizures with delta ictal onset. LTLE was observed in one patient who had 9 seizures with delta ictal onset. Scalp ictal EEG pattern was not significantly correlated with postsurgical seizure outcomes. CONCLUSIONS: Both scalp delta and theta/alpha ictal onset patterns can be commonly found in patients with MTLE. SIGNIFICANCE: Scalp delta ictal onset is not a unique EEG pattern for LTLE as commonly believed.

Interstitial Stereotactic Laser Anterior Corpus Callosotomy: A Report of 2 Cases with Operative Technique and Effectiveness.

BACKGROUND AND IMPORTANCE: Corpus callosotomy is an effective palliative treatment for medically intractable Lennox-Gastaut syndrome (LGS) that disrupts the interhemispheric synchronization of epileptiform discharges. However, traditional open corpus callosotomy carries a significant risk of surgical complications associated with craniotomy and a parafalcine approach to the corpus callosum. Here, we report 2 cases of anterior corpus callosotomy using MRI-guided stereotactic laser interstitial thermal therapy (LITT) as a minimally invasive technique for mitigating the risks of craniotomy while achieving favorable outcomes. CLINICAL PRESENTATION: Two patients with medically intractable LGS underwent stereotactic laser anterior corpus callosotomy using a 2 laser-fiber approach. Ablation of 70%-80% of the corpus callosum was confirmed by postoperative MRI diffusion tensor imaging and volumetric analysis. Marked reduction of epileptiform activity was observed in both patients during postoperative video-EEG studies as compared to preoperative video-EEG studies. Freedom from disabling seizures including drop attacks was achieved in 1 patient for 18 mo, and more than a 90% reduction of disabling seizures was achieved in the other patient for 7 mo with cognitive improvement and without surgical complications. CONCLUSION: These early data demonstrate the technical feasibility, safety, and favorable outcomes of MRI-guided stereotactic laser anterior corpus callosotomy in patients with LGS, making it a potentially safe and effective alternative to traditional open corpus callosotomy and other stereotactic methods including radiofrequency ablation and radiosurgery due to the ability to monitor the ablation in real time with MRI.

The first-hour-of-the-day sleep EEG reliably identifies interictal epileptiform discharges during long-term video-EEG monitoring.

PURPOSE: To determine the usefulness of the first-hour sleep EEG recording in identifying interictal epileptiform discharges (IEDs) during long-term video-EEG monitoring. METHOD: We retrospectively reviewed 255 consecutive patients who underwent continuous long-term video-EEG monitoring in the adult epilepsy monitoring unit (EMU) at the University of Chicago. The complete video-EEG recording was reviewed, and the occurrence of IEDs was determined for each patient. We compared the occurrence of IEDs observed during the first-hour sleep EEG recordings with the occurrence of IEDs observed during the complete video-EEG recordings. RESULTS: Overall, IEDs were observed in 134 (53%) of 255 patients during the full long-term video-EEG recording with a mean duration of 4 days. IEDs were identified in the first-hour sleep EEG in 125 (49%) of 225 patients. Comparing to reviewing full records, the first hour sleep EEG identified IEDs in 125 (93%) of 134 patients. Of the IED subtypes, the first-hour sleep EEG identified 92 (94%) of 98 patients with temporal lobe IEDs, 11 (92%) of 12 patients with frontal lobe IEDs, 3 (100%) of 3 patients with parietal lobe IEDs, 1(50%) of the 2 patients with occipital lobe IEDs, 16 (94%) of 17 patients with generalized IEDs, and 2 (100%) 2 patients with multi-focal IEDs. CONCLUSIONS: The first-hour sleep EEG reliably predicts the occurrence of IEDs during the long-term video-EEG recording, and therefore can be a time-efficient tool for identifying patients with IEDs during long-term video-EEG recording in the adult epilepsy monitoring unit.