Publications by authors named "Jorge Gonzalez-Martinez"

171 Publications

Stereotactic Electroencephalography Implantation Through Nonautologous Cranioplasty: Proof of Concept.

Oper Neurosurg (Hagerstown) 2021 Jul 22. Epub 2021 Jul 22.

Department of Neurological Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA.

Background: Stereoelectroencephalography (SEEG) is an effective method to define the epileptogenic zone (EZ) in patients with medically intractable epilepsy. Typical placement requires passing and anchoring electrodes through native skull.

Objective: To describe the successful placement of SEEG electrodes in patients without native bone. To the best of our knowledge, the use of SEEG in patients with nonautologous cranioplasties has not been described.

Methods: We describe 3 cases in which SEEG was performed through nonautologous cranioplasty. The first is a 30-yr-old male with a titanium mesh cranioplasty following a left pterional craniotomy for aneurysm clipping. The second is a 51-yr-old female who previously underwent lesionectomy of a ganglioglioma with mesh cranioplasty and subsequent recurrence of her seizures. The third is a 31-yr-old male with a polyether ether ketone cranioplasty following decompressive hemicraniectomy for trauma.

Results: SEEG was performed successfully in all three cases without intraoperative difficulties or complications and with excellent electroencephalogram recording and optimal localization of the seizure focus. The EZ was successfully localized in all three patients. There were no limitations related to drilling or inserting the guiding bolt/electrode through the nonautologous cranioplasties.

Conclusion: SEEG through nonautologous cranioplasties was clinically feasible, safe, and effective in our series. The presence of nonautologous bone cranioplasty should not preclude such patients from undergoing SEEG explorations.
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http://dx.doi.org/10.1093/ons/opab260DOI Listing
July 2021

Robotic Applications in Cranial Neurosurgery: Current and Future.

Oper Neurosurg (Hagerstown) 2021 Jun 30. Epub 2021 Jun 30.

Department of Neurosurgery, Thomas Jefferson University, Philadelphia, Pennsylvania, USA.

Robotics applied to cranial surgery is a fast-moving and fascinating field, which is transforming the practice of neurosurgery. With exponential increases in computing power, improvements in connectivity, artificial intelligence, and enhanced precision of accessing target structures, robots are likely to be incorporated into more areas of neurosurgery in the future-making procedures safer and more efficient. Overall, improved efficiency can offset upfront costs and potentially prove cost-effective. In this narrative review, we aim to translate a broad clinical experience into practical information for the incorporation of robotics into neurosurgical practice. We begin with procedures where robotics take the role of a stereotactic frame and guide instruments along a linear trajectory. Next, we discuss robotics in endoscopic surgery, where the robot functions similar to a surgical assistant by holding the endoscope and providing retraction, supplemental lighting, and correlation of the surgical field with navigation. Then, we look at early experience with endovascular robots, where robots carry out tasks of the primary surgeon while the surgeon directs these movements remotely. We briefly discuss a novel microsurgical robot that can perform many of the critical operative steps (with potential for fine motor augmentation) remotely. Finally, we highlight 2 innovative technologies that allow instruments to take nonlinear, predetermined paths to an intracranial destination and allow magnetic control of instruments for real-time adjustment of trajectories. We believe that robots will play an increasingly important role in the future of neurosurgery and aim to cover some of the aspects that this field holds for neurosurgical innovation.
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http://dx.doi.org/10.1093/ons/opab217DOI Listing
June 2021

Validation of semi-automated anatomically labeled SEEG contacts in a brain atlas for mapping connectivity in focal epilepsy.

Epilepsia Open 2021 May 6. Epub 2021 May 6.

Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, OH, USA.

Objective: Stereotactic electroencephalography (SEEG) has been widely used to explore the epileptic network and localize the epileptic zone in patients with medically intractable epilepsy. Accurate anatomical labeling of SEEG electrode contacts is critically important for correctly interpreting epileptic activity. We present a method for automatically assigning anatomical labels to SEEG electrode contacts using a 3D-segmented cortex and coregistered postoperative CT images.

Method: Stereotactic electroencephalography electrode contacts were spatially localized relative to the brain volume using a standard clinical procedure. Each contact was then assigned an anatomical label by clinical epilepsy fellows. Separately, each contact was automatically labeled by coregistering the subject's MRI to the USCBrain atlas using the BrainSuite software and assigning labels from the atlas based on contact locations. The results of both labeling methods were then compared, and a subsequent vetting of the anatomical labels was performed by expert review.

Results: Anatomical labeling agreement between the two methods for over 17 000 SEEG contacts was 82%. This agreement was consistent in patients with and without previous surgery (P = .852). Expert review of contacts in disagreement between the two methods resulted in agreement with the atlas based over manual labels in 48% of cases, agreement with manual over atlas-based labels in 36% of cases, and disagreement with both methods in 16% of cases. Labels deemed incorrect by the expert review were then categorized as either in a region directly adjacent to the correct label or as a gross error, revealing a lower likelihood of gross error from the automated method.

Significance: The method for semi-automated atlas-based anatomical labeling we describe here demonstrates potential to assist clinical workflow by reducing both analysis time and the likelihood of gross anatomical error. Additionally, it provides a convenient means of intersubject analysis by standardizing the anatomical labels applied to SEEG contact locations across subjects.
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http://dx.doi.org/10.1002/epi4.12499DOI Listing
May 2021

Radiological and Clinical Value of 7T MRI for Evaluating 3T-Visible Lesions in Pharmacoresistant Focal Epilepsies.

Front Neurol 2021 2;12:591586. Epub 2021 Mar 2.

Imaging Institute, Cleveland Clinic, Cleveland, OH, United States.

The recent FDA approval of the first 7T MRI scanner for clinical diagnostic use in October 2017 will likely increase the utilization of 7T for epilepsy presurgical evaluation. This study aims at accessing the radiological and clinical value of 7T in patients with pharmacoresistant focal epilepsy and 3T-visible lesions. Patients with pharmacoresistant focal epilepsy were included if they had a lesion on pre-operative standard-of-care 3T MRI and also a 7T research MRI. An epilepsy protocol was used for the acquisition of the 7T MRI. Prospective visual analysis of 7T MRI was performed by an experienced board-certified neuroradiologist and communicated to the patient management team. The clinical significance of the additional 7T findings was assessed by intracranial EEG (ICEEG) ictal onset, surgical resection, post-operative seizure outcome and histopathology. A subset of lesions were demarked with arrows for subsequent, retrospective comparison between 3T and 7T by 7 neuroradiologists using a set of quantitative scales: lesion presence, conspicuity, boundary, gray-white tissue contrast, artifacts, and the most helpful sequence for diagnosis. Conger's kappa for multiple raters was performed for chance-adjusted agreement statistics. A total of 47 patients were included, with the main pathology types of focal cortical dysplasia (FCD), hippocampal sclerosis, periventricular nodular heterotopia (PVNH), tumor and polymicrogyria (PMG). 7T detected additional smaller lesions in 19% (9/47) of patients, who had extensive abnormalities such as PMG and PVNH; however, these additional findings were not necessarily epileptogenic. 3T-7T comparison by the neuroradiologist team showed that lesion conspicuity and lesion boundary were significantly better at 7T ( < 0.001), particularly for FCD, PVNH and PMG. Chance-adjusted agreement was within the fair range for lesion presence, conspicuity and boundary. Gray-white contrast was significantly improved at 7T ( < 0.001). Significantly more artifacts were encountered at 7T ( < 0.001). For patients with 3T-visible lesions, 7T MRI may better elucidate the extent of multifocal abnormalities such as PVNH and PMG, providing potential targets to improve ICEEG implantation. Patients with FCD, PVNH and PMG would likely benefit the most from 7T due to improved lesion conspicuity and boundary. Pathologies in the antero-inferior temporal regions likely benefit less due to artifacts.
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http://dx.doi.org/10.3389/fneur.2021.591586DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7960771PMC
March 2021

Neurovascular networks in epilepsy: Correlating ictal blood perfusion with intracranial electrophysiology.

Neuroimage 2021 05 10;231:117838. Epub 2021 Feb 10.

Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.

Perfusion patterns observed in Subtraction Ictal SPECT Co-registered to MRI (SISCOM) assist in focus localization and surgical planning for patients with medically intractable focal epilepsy. While the localizing value of SISCOM has been widely investigated, its relationship to the underlying electrophysiology has not been extensively studied and is therefore not well understood. In the present study, we set to investigate this relationship in a cohort of 70 consecutive patients who underwent ictal and interictal SPECT studies and subsequent stereo-electroencephalography (SEEG) monitoring for localization of the epileptogenic focus and surgical intervention. Seizures recorded during SEEG evaluation (SEEG seizures) were matched to semiologically-similar seizures during the preoperative ictal SPECT evaluation (SPECT seizures) by comparing the semiological changes in the course of each seizure. The spectral changes of the ictal SEEG with respect to interictal ones over 7 traditional frequency bands (0.1 to 150Hz) were analyzed at each SEEG site. Neurovascular (SEEG/SPECT) relations were assessed by comparing the estimated spectral power density changes of the SEEG at each site with the perfusion changes (SISCOM z-scores) estimated from the acquired SISCOM map at that site. Across patients, a significant correlation (p<0.05) was observed between spectral changes during the SEEG seizure and SISCOM perfusion z-scores. Brain sites with high perfusion z-score exhibited higher increased SEEG power in theta to ripple frequency bands with concurrent suppression in delta and theta frequency bands compared to regions with lower perfusion z-score. The dynamics of the correlation of SISCOM perfusion and SEEG spectral power from ictal onset to seizure end and immediate postictal period were also derived. Forty-six (46) of the 70 patients underwent resective epilepsy surgery. SISCOM z-score and power increase in beta to ripple frequency bands were significantly higher in resected than non-resected sites in the patients who were seizure-free following surgery. This study provides for the first time concrete evidence that both hyper-perfusion and hypo-perfusion patterns observed in SISCOM maps have strong electrophysiological underpinnings, and that integration of the information from SISCOM and SEEG can shed light on the location and dynamics of the underlying epileptic brain networks, and thus advance our anatomo-electro-clinical understanding and approaches to targeted diagnostic and therapeutic interventions.
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http://dx.doi.org/10.1016/j.neuroimage.2021.117838DOI Listing
May 2021

Congress of Neurological Surgeons Systematic Review and Evidence-Based Guidelines for Deep Brain Stimulations for Obsessive-Compulsive Disorder: Update of the 2014 Guidelines.

Neurosurgery 2021 03;88(4):710-712

Department of Neurosurgery, Albany Medical College, Albany, New York, USA.

Background: In 2020, the Guidelines Task Force conducted another systematic review of the relevant literature on deep brain stimulation (DBS) for obsessive-compulsive disorder (OCD) to update the original 2014 guidelines to ensure timeliness and accuracy for clinical practice.

Objective: To conduct a systematic review of the literature and update the evidence-based guidelines on DBS for OCD.

Methods: The Guidelines Task Force conducted another systematic review of the relevant literature, using the same search terms and strategies as used to search PubMed and Embase for relevant literature. The updated search included studies published between 1966 and December 2019. The same inclusion/exclusion criteria as the original guideline were also applied. Abstracts were reviewed and relevant full-text articles were retrieved and graded. Of 864 articles, 10 were retrieved for full-text review and analysis. Recommendations were updated according to new evidence yielded by this update.

Results: Seven studies were included in the original guideline, reporting the use of bilateral DBS as more effective in improving OCD symptoms than sham treatment. An additional 10 studies were included in this update: 1 class II and 9 class III.

Conclusion: Based on the data published in the literature, the following recommendations can be made: (1) It is recommended that clinicians utilize bilateral subthalamic nucleus DBS over best medical management for the treatment of patients with medically refractory OCD (level I). (2) Clinicians may use bilateral nucleus accumbens or bed nucleus of stria terminalis DBS for the treatment of patients with medically refractory OCD (level II). There is insufficient evidence to make a recommendation for the identification of the most effective target.The full guidelines can be accessed at https://www.cns.org/guidelines/browse-guidelines-detail/deep-brain-stimulation-obsessive-compulsive-disord.
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http://dx.doi.org/10.1093/neuros/nyaa596DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8133323PMC
March 2021

Classification of Stereo-EEG Contacts in White Matter vs. Gray Matter Using Recorded Activity.

Front Neurol 2020 6;11:605696. Epub 2021 Jan 6.

Neuromedical Control Systems Lab, Institute for Computational Medicine, Biomedical Engineering, Johns Hopkins University, Baltimore, MD, United States.

For epileptic patients requiring resective surgery, a modality called stereo-electroencephalography (SEEG) may be used to monitor the patient's brain signals to help identify epileptogenic regions that generate and propagate seizures. SEEG involves the insertion of multiple depth electrodes into the patient's brain, each with 10 or more recording contacts along its length. However, a significant fraction (≈ 30% or more) of the contacts typically reside in white matter or other areas of the brain which can not be epileptogenic themselves. Thus, an important step in the analysis of SEEG recordings is distinguishing between electrode contacts which reside in gray matter vs. those that do not. MRI images overlaid with CT scans are currently used for this task, but they take significant amounts of time to manually annotate, and even then it may be difficult to determine the status of some contacts. In this paper we present a fast, automated method for classifying contacts in gray vs. white matter based only on the recorded signal and relative contact depth. We observe that bipolar referenced contacts in white matter have less power in all frequencies below 150 Hz than contacts in gray matter, which we use in a Bayesian classifier to attain an average area under the receiver operating characteristic curve of 0.85 ± 0.079 (SD) across 29 patients. Because our method gives a probability for each contact rather than a hard labeling, and uses a feature of the recorded signal that has direct clinical relevance, it can be useful to supplement decision-making on difficult to classify contacts or as a rapid, first-pass filter when choosing subsets of contacts from which to save recordings.
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http://dx.doi.org/10.3389/fneur.2020.605696DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7815703PMC
January 2021

Contributions of electrophysiology for identifying cortical language systems in patients with epilepsy.

Epilepsy Behav 2020 11 30;112:107407. Epub 2020 Sep 30.

Department of Neurological Surgery, School of Medicine, University of Pittsburgh (PA), USA; Aix-Marseille Univ, CNRS, LPC, Marseille, France. Electronic address:

A crucial element of the surgical treatment of medically refractory epilepsy is to delineate cortical areas that must be spared in order to avoid clinically relevant neurological and neuropsychological deficits postoperatively. For each patient, this typically necessitates determining the language lateralization between hemispheres and language localization within hemisphere. Understanding cortical language systems is complicated by two primary challenges: the extent of the neural tissue involved and the substantial variability across individuals, especially in pathological populations. We review the contributions made through the study of electrophysiological activity to address these challenges. These contributions are based on the techniques of magnetoencephalography (MEG), intracerebral recordings, electrical-cortical stimulation (ECS), and the electrovideo analyses of seizures and their semiology. We highlight why no single modality alone is adequate to identify cortical language systems and suggest avenues for improving current practice.
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http://dx.doi.org/10.1016/j.yebeh.2020.107407DOI Listing
November 2020

The feasibility and value of extraoperative and adjuvant intraoperative stereoelectroencephalography in rolandic and perirolandic epilepsies.

J Neurosurg Pediatr 2020 Oct 23:1-11. Epub 2020 Oct 23.

2Neurosurgery, Epilepsy Center, and.

Objective: The objective of this study was to illustrate the feasibility and value of extra- and intraoperative stereoelectroencephalography (SEEG) in patients who underwent resection in rolandic and perirolandic regions.

Methods: The authors retrospectively reviewed all consecutive patients with at least 1 year of postoperative follow-up who underwent extra- and intraoperative SEEG monitoring between January 2015 and January 2017.

Results: Four patients with pharmacoresistant rolandic and perirolandic focal epilepsy were identified, who underwent conventional extraoperative invasive SEEG evaluations followed by adjuvant intraoperative SEEG recordings. Conventional extraoperative SEEG evaluations demonstrated ictal and interictal epileptiform activities involving eloquent rolandic and perirolandic cortical areas in all patients. Following extraoperative monitoring, patients underwent preplanned staged resections guided by simultaneous and continuous adjuvant intraoperative SEEG monitoring. Resections, guided by electrode contacts of interest in 3D boundaries, were performed while continuous real-time electrographic data from SEEG recordings were obtained. Staged approaches of resections were performed until there was intraoperative resolution of synchronous rolandic/perirolandic cortex epileptic activities. All patients in the cohort achieved complete seizure freedom (Engel class IA) during the follow-up period ranging from 18 to 50 months. Resection resulted in minimal neurological deficit; 3 patients experienced transient, distal plantar flexion weakness (mild foot drop).

Conclusions: The seizure and functional outcome results of this highly preselected group of patients testifies to the feasibility and demonstrates the value of the combined benefits of both intra- and extraoperative SEEG recordings when resecting the rolandic and perirolandic areas. The novel hybrid method allows a more refined and precise identification of the epileptogenic zone. Consequently, tailored resections can be performed to minimize morbidity as well as to achieve adequate seizure control.
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http://dx.doi.org/10.3171/2020.6.PEDS2099DOI Listing
October 2020

Correlates of Attention in the Cingulate Cortex During Gambling in Humans.

Annu Int Conf IEEE Eng Med Biol Soc 2020 07;2020:2548-2551

People make decisions multiple times on a daily basis. However, some decisions are easier to make than others and perhaps require more attention to ensure a positive outcome. During gambling, one should attempt to compute the expected rewards and risks associated with decisions. Failing to allocate attention and neural resources to estimate these values can be costly, and in some cases can lead to bankruptcy. Alpha-band (8-12 Hz) oscillatory power in the brain is thought to reflect attention, but how this influences financial decision making is not well understood. Using local field potential recordings in nine human subjects performing a gambling task, we compared alpha-band power from the cingulate cortex (CC) during trials of low and high attention. We found that alpha-band power tended to be higher during a 2 second window after a fixation cue was shown in low attention trials.
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http://dx.doi.org/10.1109/EMBC44109.2020.9175499DOI Listing
July 2020

High Frequency Activity in the Orbital Frontal Cortex Modulates with Mismatched Expectations During Gambling in Humans.

Annu Int Conf IEEE Eng Med Biol Soc 2020 07;2020:1035-1038

During gambling, humans often begin by making decisions based on expected rewards and expected risks. However, expectations may not match actual outcomes. As gamblers keep track of their performance, they may feel more or less lucky, which then influences future betting decisions. Studies have identified the orbitofrontal cortex (OFC) as a brain region that plays a significant role during risky decision making in humans. However, most human studies infer neural activation from functional magnetic resonance imaging (fMRI), which has a poor temporal resolution. In particular, fMRI cannot detect activity from neuronal populations in the OFC, which may encode specific information about how a subject reacts to mismatched outcomes. In this preliminary study, four human subjects participated in a gambling task while local field potentials (LFPs), captured at a millisecond resolution, were recorded from the OFC. We analyzed high-frequency activity (HFA: >70 Hz) in the LFPs, as HFA has been shown to correlate to activation of neuronal populations. In 3 out of 4 subjects, HFA in OFC modulated between matched and mismatched trials as soon as the outcome of each bet was revealed, with modulations occurring at different times and directions depending on the anatomical location within the OFC.
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http://dx.doi.org/10.1109/EMBC44109.2020.9175721DOI Listing
July 2020

Bidirectional Interaction of Hippocampal Ripples and Cortical Slow Waves Leads to Coordinated Spiking Activity During NREM Sleep.

Cereb Cortex 2021 Jan;31(1):324-340

Department of Medicine, University of California, San Diego, La Jolla, CA 92093, USA.

The dialogue between cortex and hippocampus is known to be crucial for sleep-dependent memory consolidation. During slow wave sleep, memory replay depends on slow oscillation (SO) and spindles in the (neo)cortex and sharp wave-ripples (SWRs) in the hippocampus. The mechanisms underlying interaction of these rhythms are poorly understood. We examined the interaction between cortical SO and hippocampal SWRs in a model of the hippocampo-cortico-thalamic network and compared the results with human intracranial recordings during sleep. We observed that ripple occurrence peaked following the onset of an Up-state of SO and that cortical input to hippocampus was crucial to maintain this relationship. A small fraction of ripples occurred during the Down-state and controlled initiation of the next Up-state. We observed that the effect of ripple depends on its precise timing, which supports the idea that ripples occurring at different phases of SO might serve different functions, particularly in the context of encoding the new and reactivation of the old memories during memory consolidation. The study revealed complex bidirectional interaction of SWRs and SO in which early hippocampal ripples influence transitions to Up-state, while cortical Up-states control occurrence of the later ripples, which in turn influence transition to Down-state.
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http://dx.doi.org/10.1093/cercor/bhaa228DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8179633PMC
January 2021

Value of 7T MRI and post-processing in patients with nonlesional 3T MRI undergoing epilepsy presurgical evaluation.

Epilepsia 2020 11 19;61(11):2509-2520. Epub 2020 Sep 19.

Imaging Institute, Cleveland Clinic, Cleveland, OH, USA.

Objective: Ultra-high-field 7-Tesla (7T) magnetic resonance imaging (MRI) offers increased signal-to-noise and contrast-to-noise ratios, which may improve visualization of cortical malformations. We aim to assess the clinical value of in vivo structural 7T MRI and its post-processing for the noninvasive identification of epileptic brain lesions in patients with pharmacoresistant epilepsy and nonlesional 3T MRI who are undergoing presurgical evaluation.

Methods: Sixty-seven patients were included who had nonlesional 3T MRI by official radiology report. Epilepsy protocols were used for the 3T and 7T acquisitions. Post-processing of the 7T T1-weighted magnetization-prepared two rapid acquisition gradient echoes sequence was performed using the morphometric analysis program (MAP) with comparison to a normal database consisting of 50 healthy controls. Review of 7T was performed by an experienced board-certified neuroradiologist and at the multimodal patient management conference. The clinical significance of 7T findings was assessed based on intracranial electroencephalography (ICEEG) ictal onset, surgery, postoperative seizure outcomes, and histopathology.

Results: Unaided visual review of 7T detected previously unappreciated subtle lesions in 22% (15/67). When aided by 7T MAP, the total yield increased to 43% (29/67). The location of the 7T-identified lesion was identical to or contained within the ICEEG ictal onset in 13 of 16 (81%). Complete resection of the 7T-identified lesion was associated with seizure freedom (P = .03). Histopathology of the 7T-identified lesions encountered mainly focal cortical dysplasia (FCD). 7T MAP yielded 25% more lesions (6/24) than 3T MAP, and showed improved conspicuity in 46% (11/24).

Significance: Our data suggest a major benefit of 7T with post-processing for detecting subtle FCD lesions for patients with pharmacoresistant epilepsy and nonlesional 3T MRI.
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http://dx.doi.org/10.1111/epi.16682DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7722133PMC
November 2020

The Stereoelectroencephalography Methodology Applied to Epilepsies with a Visible Lesion.

Neurosurg Clin N Am 2020 Jul;31(3):387-394

Cleveland Clinic Lerner College of Medicine, Cleveland, OH, USA.

Resective epilepsy surgery relies on accurate preoperative localization of the epileptogenic zone (EZ), so presurgical evaluation is necessary to obtain the most accurate information from clinical, anatomic, and neurophysiologic aspects, with the ultimate goal of performing an individualized surgical treatment. The noninvasive methods of seizure localization are complementary and results must be interpreted in conjunction, in an attempt to compose localization hypotheses of the anatomic location of the EZ. Stereoelectroencephalography is an extraoperative invasive method that is applied in patients with medically refractory focal epilepsy in order to anatomically define the EZ and the related functional cortical areas.
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http://dx.doi.org/10.1016/j.nec.2020.03.010DOI Listing
July 2020

The FAST graph: A novel framework for the anatomically-guided visualization and analysis of cortico-cortical evoked potentials.

Epilepsy Res 2020 03 9;161:106264. Epub 2020 Jan 9.

Department of Neurology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX 77030, USA.

Background: Intracerebral electroencephalography (iEEG) using stereoelectroencephalography (SEEG) methodology for epilepsy surgery gives rise to complex data sets. The neurophysiological data obtained during the in-patient period includes categorization of the evoked potentials resulting from direct electrical cortical stimulation such as cortico-cortical evoked potentials (CCEPs). These potentials are recorded by hundreds of contacts, making these waveforms difficult to quickly interpret over such high-density arrays that are organized in three dimensional fashion.

New Method: The challenge in analyzing CCEPs data arises not just from the density of the array, but also from the stimulation of a number of different intracerebral sites. A systematic methodology for visualization and analysis of these evoked data is lacking. We describe the process of incorporating anatomical information into the visualizations, which are then compared to more traditional plotting techniques to highlight the usefulness of the new framework.

Results: We describe here an innovative framework for sorting, registering, labeling, ordering, and quantifying the functional CCEPs data, using the anatomical labelling of the brain, to provide an informative visualization and summary statistics which we call the "FAST graph" (Functional-Anatomical STacked area graphs). The FAST graph analysis is used to depict the significant CCEPs responses in patient with focal epilepsy.

Conclusions: The novel plotting approach shown here allows us to visualize high-density stimulation data in a single summary plot for subsequent detailed analyses. Improving the visual presentation of complex data sets aides in enhancing the clinical utility of the data.
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http://dx.doi.org/10.1016/j.eplepsyres.2020.106264DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7206791PMC
March 2020

Estimating Intracranial EEG Signals at Missing Electrodes in Epileptic Networks.

Annu Int Conf IEEE Eng Med Biol Soc 2019 Jul;2019:3858-3861

Epilepsy can be controlled by targeted treatment of the epileptogenic zone (EZ), the region in the brain where seizures originate. Identification of the EZ often requires visual inspection of invasive EEG recordings and thus relies heavily on placement of electrodes, such that they cover the EZ. A dense brain coverage would be ideal to obtain accurate boundaries of the EZ but is not possible due to surgical limitations. This gives rise to the "missing electrode problem", where clinicians desire to know what neural activity looks like between implanted electrodes. In this paper, we compare two methods for time series estimation of missing stereotactic EEG (SEEG) recordings. Specifically, we represent SEEG data as a sequence of Linear Time-Invariant (LTI) models. We then remove one signal from the data set and apply two different algorithms to simultaneously estimate the LTI models and the "missing" signal: (i) a Reduced-Order Observer in combination with Least Squares Estimation and (ii) an Expectation Maximization based Kalman Filter. The performance of each approach is evaluated in terms of (i) estimation error, (ii) sensitivity to initial conditions, and (iii) algorithm run-time. We found that the EM approach has smaller estimation errors and is less sensitive to initial conditions. However, the reduced-order observer has a run-time that is orders of magnitude faster.
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http://dx.doi.org/10.1109/EMBC.2019.8856601DOI Listing
July 2019

Neural Activity from Attention Networks Predicts Movement Errors.

Annu Int Conf IEEE Eng Med Biol Soc 2019 Jul;2019:2149-2152

Traditionally, movement-related behavior is estimated using activity from motor regions in the brain. This predictive capability of interpreting neural signals into tangible outputs has led to the emergence of Brain-Computer Interface (BCI) systems. However, nonmotor regions can play a significant role in shaping how movements are executed. Our goal was to explore the contribution of nonmotor brain regions to movement using a unique experimental paradigm in which local field potential recordings of several cortical and subcortical regions were obtained from eight epilepsy patients implanted with depth electrodes as they performed goal-directed reaching movements. The instruction of the task was to move a cursor with a robotic arm to the indicated target with a specific speed, where correct trials were ones in which the subject achieved the instructed speed. We constructed subject-specific models that predict the speed error of each trial from neural activity in nonmotor regions. Neural features were found by averaging spectral power of activity in multiple frequency bands produced during the planning or execution of movement. Features with high predictive power were selected using a forward selection greedy search. Using our modeling framework, we were able to identify networks of regions related to attention that significantly contributed to predicting trial errors. Our results suggest that nonmotor brain regions contain relevant information about upcoming movements and should be further studied.
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http://dx.doi.org/10.1109/EMBC.2019.8856958DOI Listing
July 2019

Neural Correlates of Internal States that Capture Movement Variability.

Annu Int Conf IEEE Eng Med Biol Soc 2019 Jul;2019:534-537

The brain lacks the ability to perfectly replicate movements. In particular, if specific movements are cued sequentially, how you perform on past trials may influence how you move on current and future trials. Past trial outcomes may, for example, modulate motivation or attention which can play a significant role in how one moves, yet variability due to such internal factors are often ignored when modeling the sensorimotor control system. In this study, we wish to extract such internal factors by modeling variability in movements during a motor task riddled with unpredictable perturbations. Four subjects performed the task, and we simultaneously obtained Local Field Potential (LFP) activity from nonmotor brain regions via depth electrodes implanted for clinical purposes. We first show that motor behavior depends not only on current trial conditions, but also on internal state variables that accumulate past outcomes involving movement performance, movement speed, and whether or not perturbations have occurred. We further show that these internal states modulate with beta band activity in specific brain regions on a trial-by-trial basis. These results suggest a nontraditional role of nonmotor brain regions and prompt a need for further exploration.
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http://dx.doi.org/10.1109/EMBC.2019.8856778DOI Listing
July 2019

Emerging roles of network analysis for epilepsy.

Epilepsy Res 2020 01 9;159:106255. Epub 2019 Dec 9.

Department of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, CA, United States.

In recent years there has been increasing interest in applying network science tools to EEG data. At the 2018 American Epilepsy Society conference in New Orleans, LA, the yearly session of the Engineering and Neurostimulation Special Interest Group focused on emerging, translational technologies to analyze seizure networks. Each speaker demonstrated practical examples of how network tools can be utilized in clinical care and provide additional data to help care for patients with intractable epilepsy. The groups presented advances using tools from functional connectivity, control theory, and graph theory to analyze human EEG data. These tools have great potential to augment clinical interpretation of EEG signals.
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http://dx.doi.org/10.1016/j.eplepsyres.2019.106255DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6990460PMC
January 2020

Incorporating New Technology Into a Surgical Technique: The Learning Curve of a Single Surgeon's Stereo-Electroencephalography Experience.

Neurosurgery 2020 03;86(3):E281-E289

Epilepsy Center, Cleveland Clinic, Cleveland, Ohio.

Background: Technological improvements frequently outpace the publication of randomized, controlled trials in surgical patients. This makes the application of new surgical techniques difficult as surgeons solely use clinical experience to guide changes in their practice.

Objective: To quantitatively examine the learning curve of incorporating new technology into a surgical technique and discuss the clinical significance of incorporating this new technology into daily practice. To identify areas of improvement for operative efficiency and safety.

Methods: A retrospective observational study examining quantitative measures of operative efficiency and safety from 2009 to 2017 in 454 consecutive patients undergoing stereo-electroencephalography depth electrode implantations.

Results: The transition to a new robotic technique significantly improved operative times (196 min [95% CI 173-219] vs 115 min [95% CI 111-118], P < .0001). Cumulative sum (CUSUM) analysis demonstrated that mastery of the robotic technique took much longer than the frame-based technique (operative time peak at case 75 vs case 25, plateau of 150 vs 10 cases). Although hemorrhage rates using different vascular imaging techniques did not appear to differ using traditional statistical analysis (magnetic resonance imaging, MRI 22.3%, computed tomography angiography, CTA 17.9%, angiogram 18.1%, likelihood ratio χ2 = 4.84, P = .30), CUSUM analysis suggested MRI as the vascular imaging modality leading to higher hemorrhage and symptomatic hemorrhage rates at our center.

Conclusion: This experience demonstrates an improvement in operative efficiency through a series of changes made using clinical experience and intuition while transitioning to a completely new paradigm. CUSUM analysis identified potential areas for improvement in both operative efficiency and safety if used in a prospective manner.
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http://dx.doi.org/10.1093/neuros/nyz498DOI Listing
March 2020

Improved identification and differentiation from epileptiform activity of human hippocampal sharp wave ripples during NREM sleep.

Hippocampus 2020 06 25;30(6):610-622. Epub 2019 Nov 25.

Department of Neurosciences, University of California at San Diego, La Jolla, California.

In rodents, pyramidal cell firing patterns from waking may be replayed in nonrapid eye movement sleep (NREM) sleep during hippocampal sharp wave ripples (HC-SWR). In humans, HC-SWR have only been recorded with electrodes implanted to localize epileptogenicity. Here, we characterize human HC-SWR with rigorous rejection of epileptiform activity, requiring multiple oscillations and coordinated sharp waves. We demonstrated typical SWR in those rare HC recordings which lack interictal epileptiform spikes (IIS) and with no or minimal seizure involvement. These HC-SWR have a similar rate (~12 min on average, variable across NREM stages and anterior/posterior HC) and apparent intra-HC topography (ripple maximum in putative stratum pyramidale, slow wave in radiatum) as rodents, though with lower frequency (~85 Hz compared to ~140 Hz in rodents). Similar SWR are found in HC with IIS, but no significant seizure involvement. These SWR were modulated by behavior, being largely absent (<2 min ) except during NREM sleep in both Stage 2 (~9 min ) and Stage 3 (~15 min ), distinguishing them from IIS. This study quantifies the basic characteristics of a strictly selected sample of SWR recorded in relatively healthy human hippocampi.
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http://dx.doi.org/10.1002/hipo.23183DOI Listing
June 2020

Hemispherectomy in adults and adolescents: Seizure and functional outcomes in 47 patients.

Epilepsia 2019 12 2;60(12):2416-2427. Epub 2019 Nov 2.

Epilepsy Center, Cleveland Clinic, Cleveland, Ohio.

Objective: To examine longitudinal seizure and functional outcomes after hemispherectomy in adults and adolescents.

Methods: We reviewed 47 consecutive patients older than 16 years who underwent hemispherectomy between 1996 and 2016 at our center. Clinical, electroencephalographic (EEG), imaging, neuropsychological, surgical, and functional status data were analyzed.

Results: Thirty-six patients were 18 years or older at surgery; 11 were aged between 16 and 18 years. Brain injury leading to hemispheric epilepsy occurred before 10 years of age in 41 (87%) patients. At a mean follow-up of 5.3 postoperative years (median = 2.9 years), 36 (77%) had Engel class I outcome. Longitudinal outcome analysis showed 84% seizure freedom (Engel IA) at 6 months, 76% at 2 years, and 76% at 5 years and beyond, with stable longitudinal outcomes up to 12 years from surgery. Multivariate analysis demonstrated that acute postoperative seizures and contralateral interictal spikes at 6-month follow-up EEG were associated with seizure recurrence. Patients who could walk unaided preoperatively and had no cerebral peduncle atrophy on brain magnetic resonance imaging were more likely to experience worsening of motor function postoperatively. Otherwise, postoperative ambulatory status and hand function were unchanged. Of the 19 patients who completed neuropsychological testing, 17 demonstrated stable or improved postoperative outcomes.

Significance: Hemispherectomy in adults is a safe and effective procedure, with seizure freedom rates and functional outcome similar to those observed in children.
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http://dx.doi.org/10.1111/epi.16378DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6911022PMC
December 2019

Learning to define an electrical biomarker of the epileptogenic zone.

Hum Brain Mapp 2020 02 14;41(2):429-441. Epub 2019 Oct 14.

Epilepsy Center, Cleveland Clinic Neurological Institute, Cleveland, Ohio.

The role of fast activity as a potential biomarker in localization of the epileptogenic zone (EZ) remains controversial due to recently reported unsatisfactory performance. We recently identified a "fingerprint" of the EZ as a time-frequency pattern that is defined by a combination of preictal spike(s), fast oscillatory activity, and concurrent suppression of lower frequencies. Here we examine the generalizability of the fingerprint in application to an independent series of patients (11 seizure-free and 13 non-seizure-free after surgery) and show that the fingerprint can also be identified in seizures with lower frequency (such as beta) oscillatory activity. In the seizure-free group, only 5 of 47 identified EZ contacts were outside the resection. In contrast, in the non-seizure-free group, 104 of 142 identified EZ contacts were outside the resection. We integrated the fingerprint prediction with the subject's MR images, thus providing individualized anatomical estimates of the EZ. We show that these fingerprint-based estimates in seizure-free patients are almost always inside the resection. On the other hand, for a large fraction of the nonseizure-free patients the estimated EZ was not well localized and was partially or completely outside the resection, which may explain surgical failure in such cases. We also show that when mapping fast activity alone onto MR images, the EZ was often over-estimated, indicating a reduced discriminative ability for fast activity relative to the full fingerprint for localization of the EZ.
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http://dx.doi.org/10.1002/hbm.24813DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7268034PMC
February 2020

Coordination of Human Hippocampal Sharpwave Ripples during NREM Sleep with Cortical Theta Bursts, Spindles, Downstates, and Upstates.

J Neurosci 2019 10 18;39(44):8744-8761. Epub 2019 Sep 18.

Department of Neurosciences,

In rodents, waking firing patterns replay in NREM sleep during hippocampal sharpwave ripples (HC-SWRs), correlated with neocortical graphoelements (NC-GEs). NC-GEs include theta bursts, spindles, downstates, and upstates. In humans, consolidation during sleep is correlated with scalp-recorded spindles and downstates/upstates, but HC-SWRs cannot be recorded noninvasively. Here we show in humans of both sexes that HC-SWRs are highly correlated with NC-GEs during NREM, with significantly more related HC-SWRs/NC-GEs for downstates or upstates than theta bursts or spindles, in N2 than N3, in posterior than anterior HC, in frontal than occipital cortex, and ipsilaterally than contralaterally. The preferences interacted (e.g., frontal spindles co-occurred frequently with posterior HC-SWRs in N2). These preferred GEs, stages, and locations for HC-SWR/NC-GE interactions may index selective consolidation activity, although that was not tested in this study. SWR recorded in different HC regions seldom co-occurred, and were related to GE in different cortical areas, showing that HC-NC interact in multiple transient, widespread but discrete, networks. NC-GEs tend to occur with consistent temporal relationships to HC-SWRs, and to each other. Cortical theta bursts usually precede HC-SWRs, where they may help define cortical input triggering HC-SWR firing. HC-SWRs often follow cortical downstate onsets, surrounded by locally decreased broadband power, suggesting a mechanism synchronizing cortical, thalamic, and hippocampal activities. Widespread cortical upstates and spindles follow HC-SWRs, consistent with the hypothesized contribution by hippocampal firing during HC-SWRs to cortical firing-patterns during upstates and spindles. Overall, our results describe how hippocampal and cortical oscillations are coordinated in humans during events that are critical for memory consolidation in rodents. Hippocampal sharpwave ripples, essential for memory consolidation, mark when hippocampal neurons replay waking firing patterns. In rodents, cortical sleep waves coordinate the transfer of temporary hippocampal to permanent cortical memories, but their relationship with human hippocampal sharpwave ripples remains unclear. We show that human hippocampal sharpwave ripples co-occur with all varieties of cortical sleep waves, in all cortical regions, and in all stages of NREM sleep, but with overall preferences for each of these. We found that sharpwave ripples in different parts of the hippocampus usually occurred independently of each other, and preferentially interacted with different cortical areas. We found that sharpwave ripples typically occur after certain types of cortical waves, and before others, suggesting how the cortico-hippocampo-cortical interaction may be organized in time and space.
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http://dx.doi.org/10.1523/JNEUROSCI.2857-18.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6820213PMC
October 2019

Posterior Hippocampal Spindle Ripples Co-occur with Neocortical Theta Bursts and Downstates-Upstates, and Phase-Lock with Parietal Spindles during NREM Sleep in Humans.

J Neurosci 2019 11 17;39(45):8949-8968. Epub 2019 Sep 17.

Department of Neurosciences and

Human anterior and posterior hippocampus (aHC, pHC) differ in connectivity and behavioral correlates. Here we report physiological differences in humans of both sexes. During NREM sleep, the human hippocampus generates sharpwave ripples (SWRs) similar to those which in rodents mark memory replay. We show that while pHC generates SWRs, it also generates approximately as many spindle ripples (SSR: ripples phase-locked to local spindles). In contrast, SSRs are rare in aHC. Like SWRs, SSRs often co-occur with neocortical theta bursts (TBs), downstates (DSs), sleep spindles (SSs), and upstates (USs), which coordinate cortico-hippocampal interactions and facilitate consolidation in rodents. SWRs co-occur with these waves in widespread cortical areas, especially frontocentral. These waves typically occur in the sequence TB-DS-SS-US, with SWRs usually occurring before SS-US. In contrast, SSRs occur ∼350 ms later, with a strong preference for co-occurrence with posterior-parietal SSs. pHC-SSs were strongly phase-locked with parietal-SSs, and pHC-SSRs were phase-coupled with pHC-SSs and parietal-SSs. Human SWRs (and associated replay events, if any) are separated by ∼5 s on average, whereas ripples on successive SSR peaks are separated by only ∼80 ms. These distinctive physiological properties of pHC-SSR enable an alternative mechanism for hippocampal engagement with neocortex. Rodent hippocampal neurons replay waking events during sharpwave ripples (SWRs) in NREM sleep, facilitating memory transfer to a permanent cortical store. We show that human anterior hippocampus also produces SWRs, but spindle ripples predominate in posterior. Whereas SWRs typically occur as cortex emerges from inactivity, spindle ripples typically occur at peak cortical activity. Furthermore, posterior hippocampal spindle ripples are tightly coupled to posterior parietal locations activated by conscious recollection. Finally, multiple spindle ripples can recur within a second, whereas SWRs are separated by ∼5 s. The human posterior hippocampus is considered homologous to rodent dorsal hippocampus, which is thought to be specialized for consolidation of specific memory details. We speculate that these distinct physiological characteristics of posterior hippocampal spindle ripples may support a related function in humans.
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http://dx.doi.org/10.1523/JNEUROSCI.2858-18.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6832672PMC
November 2019

(Re)Defining success in epilepsy surgery: The importance of relative seizure reduction in patient-reported quality of life.

Epilepsia 2019 10 28;60(10):2078-2085. Epub 2019 Aug 28.

Epilepsy Center, Cleveland Clinic, Cleveland, Ohio.

Objective: Previous work has suggested that seizure outcome is the most important predictor of quality of life (QoL) after epilepsy surgery, but it is unknown which specific seizure outcome measure should be used in judging surgical success. We assess three different seizure outcome measures (relative seizure reduction, absolute seizure reduction, and seizure freedom [yes/no]) to investigate which measure best predicts postoperative QoL.

Methods: We prospectively surveyed patients at outpatient visits before and after epilepsy surgery (n = 550). The QoL measure was the Quality of Life in Epilepsy (QOLIE-10) score at the patient's most recent office visit. We created multivariate regression models to predict postoperative QOLIE-10, with a different seizure outcome measure in each model. We compared models using adjusted R values and Akaike information criteria (AIC).

Results: Our cohort had a high level of disease severity and complexity (17% repeat surgery, 39% extratemporal, and 18% nonlesional). For the cohort as a whole, mean absolute seizure frequency decreased from 1 per day to 0.1 per day (P < .001), and mean reduction was 73% (95% confidence interval [CI] 66%-81%). Average improvement in QoL score was 5.3 (95% CI 4.1-6.5) points. Of patients who reported an improvement in QoL, 27% had persistent seizures. Comparison of regression models to predict QoL showed that the worst model was provided when using "absolute seizure reduction," but that models using "relative seizure reduction" and "seizure freedom (yes/no)" were equally strong.

Significance: In our high severity and complexity cohort, a substantial subset of patients (27%) reported improved QoL despite persistent seizures. Relative seizure reduction was at least as good a predictor of QoL as seizure freedom. A yes/no seizure freedom variable may be a suboptimal measure of surgical success, especially in high complexity cohorts.
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http://dx.doi.org/10.1111/epi.16327DOI Listing
October 2019

Connectivity of the human insula: A cortico-cortical evoked potential (CCEP) study.

Cortex 2019 11 18;120:419-442. Epub 2019 Jun 18.

Epilepsy Center, Cleveland Clinic, Neurological Institute, Cleveland, OH, USA.

Objective: The human insula is increasingly being implicated as a multimodal functional network hub involved in a large variety of complex functions. Due to its inconspicuous location and highly vascular anatomy, it has historically been difficult to study. Cortico-cortical evoked potentials (CCEPs), utilize low frequency stimulation to map cerebral networks. They were used to study connections of the human insula.

Methods: CCEP data was acquired from each sub-region of the dominant and non-dominant insula in 30 patients who underwent stereo-EEG. Connectivity strength to the various cortical regions was obtained via a measure of root mean square (RMS), calculated from each gyrus of the insula and ranked into weighted means.

Results: The results of all cumulative CCEP responses for each individual gyrus were represented by circro plots. Forty-nine individual CCEP pairs were stimulated across all the gyri from the right and left insula. In brief, the left insula contributed more greatly to language areas. Sensory function, pain, saliency processing and vestibular function were more heavily implicated from the right insula. Connections to the primary auditory cortex arose from both insula regions. Both posterior insula regions showed significant contralateral connectivity. Ipsilateral mesial temporal connections were seen from both insula regions. In visual function, we further report the novel finding of a direct connection between the right posterior insula and left visual cortex.

Significance: The insula is a major multi-modal network hub with the cerebral cortex having major roles in language, sensation, auditory, visual, limbic and vestibular functions as well as saliency processing. In temporal lobe epilepsy surgery failure, the insula may be implicated as an extra temporal cause, due to the strong mesial temporal connectivity findings.
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http://dx.doi.org/10.1016/j.cortex.2019.05.019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6825888PMC
November 2019

Tracking a changing paradigm and the modern face of epilepsy surgery: A comprehensive and critical review on the hunt for the optimal extent of resection in mesial temporal lobe epilepsy.

Epilepsia 2019 09 13;60(9):1768-1793. Epub 2019 Aug 13.

Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, Ohio.

Surgical management of medically intractable epilepsy was historically based on the premise of excising the presumed substrate of disease, that is, "the epileptogenic zone." There was early interest in establishing the extent of resection of the temporal lobe that optimized postoperative reduction in seizure burden while preserving neurocognitive function. Studies approaching this question used varied methods of defining and measuring "extent," complicating the task of distilling evidence-based recommendations for surgical practice. A palpable shift in the paradigm of surgical epilepsy has gained traction and greatly altered not only the kind of studies being undertaken but the focus of inquiry itself. Key to this paradigm shift has been the increasingly well-held notion that epilepsy, far from being a disease of a single problem focus, is rather a disease of a problem network. Where a former generation of investigators labored to find an optimal extent of resection, concentrating on magnetic resonance imaging-visible lesions and on standardization of the extent of resection (ie, "standard temporal lobectomy"), the modern strategy is more concerned with understanding network activation and its concordance with presurgical clinical and electrophysiological features and the organization of epileptic activity over time. The vital lessons of the early literature investigating optimal extent of resection, however, remain informative to the field, and it is worthwhile to contextualize them within the modern network-focused paradigm. In this comprehensive review of the literature, we aim to recapitulate the major findings of the "optimal extent of resection" literature (focusing on both seizure control and neuropsychological outcomes) and distill wherever possible the consensus findings that may guide surgical approach to epileptic disease of the temporal lobe. We also review the particular implications of modern laser ablation techniques on the question of "optimal extent of resection" in temporal lobe epilepsy, and contextualize them as a marker of a shifting paradigm.
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http://dx.doi.org/10.1111/epi.16310DOI Listing
September 2019
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