Publications by authors named "Jonathan P Miller"

85 Publications

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

The Neural Representation of Force across Grasp Types in Motor Cortex of Humans with Tetraplegia.

eNeuro 2021 Jan-Feb;8(1). Epub 2021 Feb 19.

Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH 44106

Intracortical brain-computer interfaces (iBCIs) have the potential to restore hand grasping and object interaction to individuals with tetraplegia. Optimal grasping and object interaction require simultaneous production of both force and grasp outputs. However, since overlapping neural populations are modulated by both parameters, grasp type could affect how well forces are decoded from motor cortex in a closed-loop force iBCI. Therefore, this work quantified the neural representation and offline decoding performance of discrete hand grasps and force levels in two human participants with tetraplegia. Participants attempted to produce three discrete forces (light, medium, hard) using up to five hand grasp configurations. A two-way Welch ANOVA was implemented on multiunit neural features to assess their modulation to and Demixed principal component analysis (dPCA) was used to assess for population-level tuning to force and grasp and to predict these parameters from neural activity. Three major findings emerged from this work: (1) force information was neurally represented and could be decoded across multiple hand grasps (and, in one participant, across attempted elbow extension as well); (2) grasp type affected force representation within multiunit neural features and offline force classification accuracy; and (3) grasp was classified more accurately and had greater population-level representation than force. These findings suggest that force and grasp have both independent and interacting representations within cortex, and that incorporating force control into real-time iBCI systems is feasible across multiple hand grasps if the decoder also accounts for grasp type.
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http://dx.doi.org/10.1523/ENEURO.0231-20.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7920535PMC
June 2021

Connectivity-based identification of a potential neurosurgical target for mood disorders.

J Psychiatr Res 2020 06 21;125:113-120. Epub 2020 Mar 21.

Case Western Reserve University, USA.

Objective: Stereotactic ablation (cingulotomy) and subcallosal cingulate deep brain stimulation (SCC DBS) of different regions of the cingulum bundle (CB) have been successfully used to treat psychiatric disorders, such as depression and bipolar disorder. They are hypothesized to work by disrupting white matter pathways involved in the clinical manifestation of these disorders. This study aims to compare the connectivity of different CB subregions using tractography to evaluate stereotactic targets for the treatment of mood disorders.

Methods: Fourteen healthy volunteers underwent 3T-MR imaging followed by connectivity analysis using probabilistic tractography. Twenty-one anatomic regions of interest were defined for each subject: 10 CB subregions (including the classical cingulotomy and SCC DBS targets) and 11 cortical/subcortical structures implicated in mood disorders. Connectivity results were compared using Friedman and Bonferroni-corrected post-hoc Wilcoxon tests.

Results: CB connectivity showed a high degree of regional specificity. Both of the traditional stereotactic targets had widespread connectivity with discrete topology. The cingulotomy target connected primarily to the dorsomedial frontal, dorsal anterior cingulate, and posterior cingulate cortices, whereas the SCC DBS target connected mostly to the subgenual anterior cingulate and medial/central orbitofrontal cortices. However, a region of the rostral dorsal CB, lying between these surgical targets, encompassed statistically equivalent connections to all five cortical regions.

Conclusions: The CB is associated with brain structures involved in affective disorders, and the rostral dorsal CB demonstrates connectivity that is comparable to the combined connectivity of cingulotomy and SCC DBS neurosurgical interventions. The rostral dorsal CB represents a surgical target worthy of clinical exploration for mood disorders.
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http://dx.doi.org/10.1016/j.jpsychires.2020.03.011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7183327PMC
June 2020

Neural Representation of Observed, Imagined, and Attempted Grasping Force in Motor Cortex of Individuals with Chronic Tetraplegia.

Sci Rep 2020 01 29;10(1):1429. Epub 2020 Jan 29.

Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH, 44016, USA.

Hybrid kinetic and kinematic intracortical brain-computer interfaces (iBCIs) have the potential to restore functional grasping and object interaction capabilities in individuals with tetraplegia. This requires an understanding of how kinetic information is represented in neural activity, and how this representation is affected by non-motor parameters such as volitional state (VoS), namely, whether one observes, imagines, or attempts an action. To this end, this work investigates how motor cortical neural activity changes when three human participants with tetraplegia observe, imagine, and attempt to produce three discrete hand grasping forces with the dominant hand. We show that force representation follows the same VoS-related trends as previously shown for directional arm movements; namely, that attempted force production recruits more neural activity compared to observed or imagined force production. Additionally, VoS-modulated neural activity to a greater extent than grasping force. Neural representation of forces was lower than expected, possibly due to compromised somatosensory pathways in individuals with tetraplegia, which have been shown to influence motor cortical activity. Nevertheless, attempted forces (but not always observed or imagined forces) could be decoded significantly above chance, thereby potentially providing relevant information towards the development of a hybrid kinetic and kinematic iBCI.
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http://dx.doi.org/10.1038/s41598-020-58097-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6989675PMC
January 2020

Neural ensemble dynamics in dorsal motor cortex during speech in people with paralysis.

Elife 2019 12 10;8. Epub 2019 Dec 10.

Department of Neurosurgery, Stanford University, Stanford, United States.

Speaking is a sensorimotor behavior whose neural basis is difficult to study with single neuron resolution due to the scarcity of human intracortical measurements. We used electrode arrays to record from the motor cortex 'hand knob' in two people with tetraplegia, an area not previously implicated in speech. Neurons modulated during speaking and during non-speaking movements of the tongue, lips, and jaw. This challenges whether the conventional model of a 'motor homunculus' division by major body regions extends to the single-neuron scale. Spoken words and syllables could be decoded from single trials, demonstrating the potential of intracortical recordings for brain-computer interfaces to restore speech. Two neural population dynamics features previously reported for arm movements were also present during speaking: a component that was mostly invariant across initiating different words, followed by rotatory dynamics during speaking. This suggests that common neural dynamical motifs may underlie movement of arm and speech articulators.
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http://dx.doi.org/10.7554/eLife.46015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6954053PMC
December 2019

The p53 inactivators pifithrin-μ and pifithrin-α mitigate TBI-induced neuronal damage through regulation of oxidative stress, neuroinflammation, autophagy and mitophagy.

Exp Neurol 2020 02 26;324:113135. Epub 2019 Nov 26.

Graduate Institute of Medical Sciences, College of Medicine, Taipei Medical University, Taipei 110, Taiwan; Department of Neurosurgery, Taipei Medical University Hospital, Taipei 110, Taiwan; Neuroscience Research Center, Taipei Medical University, Taipei 110, Taiwan. Electronic address:

Traumatic brain injury (TBI) is one of the most common causes of death and disability worldwide. We investigated whether inhibition of p53 using pifithrin (PFT)-α or PFT-μ provides neuroprotective effects via p53 transcriptional dependent or -independent mechanisms, respectively. Sprague Dawley rats were subjected to controlled cortical impact TBI followed by the administration of PFTα or PFT-μ (2 mg/kg, i.v.) at 5 h after TBI. Brain contusion volume, as well as sensory and motor functions were evaluated at 24 h after TBI. TBI-induced impairments were mitigated by both PFT-α and PFT-μ. Fluoro-Jade C staining was used to label degenerating neurons within the TBI-induced cortical contusion region that, together with Annexin V positive neurons, were reduced by PFT-μ. Double immunofluorescence staining similarly demonstrated that PFT-μ significantly increased HO-1 positive neurons and mRNA expression in the cortical contusion region as well as decreased numbers of 4-hydroxynonenal (4HNE)-positive cells. Levels of mRNA encoding for p53, autophagy, mitophagy, anti-oxidant, anti-inflammatory related genes and proteins were measured by RT-qPCR and immunohistochemical staining, respectively. PFT-α, but not PFT-μ, significantly lowered p53 mRNA expression. Both PFT-α and PFT-μ lowered TBI-induced pro-inflammatory cytokines (IL-1β and IL-6) mRNA levels as well as TBI-induced autophagic marker localization (LC3 and p62). Finally, treatment with PFT-μ mitigated TBI-induced declines in mRNA levels of PINK-1 and SOD2. Our data suggest that both PFT-μ and PFT-α provide neuroprotective actions through regulation of oxidative stress, neuroinflammation, autophagy, and mitophagy mechanisms, and that PFT-μ, in particular, holds promise as a TBI treatment strategy.
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http://dx.doi.org/10.1016/j.expneurol.2019.113135DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7792017PMC
February 2020

The Reconnecting the Hand and Arm with Brain (ReHAB) Commentary on "An Integrated Brain-Machine Interface Platform With Thousands of Channels".

J Med Internet Res 2019 10 31;21(10):e16339. Epub 2019 Oct 31.

Case Western Reserve University, University Hospitals Cleveland Medical Center, Cleveland, OH, United States.

Intracortical brain-machine interfaces are a promising technology for allowing people with chronic and severe neurological disorders that resulted in loss of function to potentially regain those functions through neuroprosthetic devices. The penetrating microelectrode arrays used in almost all previous studies of intracortical brain-machine interfaces in people had a limited recording life (potentially due to issues with long-term biocompatibility), as well as a limited number of recording electrodes with limited distribution in the brain. Significant advances are required in this array interface to deal with the issues of long-term biocompatibility and lack of distributed recordings. The Musk and Neuralink manuscript proposes a novel and potentially disruptive approach to advancing the brain-electrode interface technology, with the potential of addressing many of these hurdles. Our commentary addresses the potential advantages of the proposed approach, as well as the remaining challenges to be addressed.
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http://dx.doi.org/10.2196/16339DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6914246PMC
October 2019

Facial Sensory Restoration After Trigeminal Sensory Rhizotomy by Collateral Sprouting From the Occipital Nerves.

Neurosurgery 2020 05;86(5):E436-E441

School of Medicine, Case Western Reserve University, Cleveland, Ohio.

Background And Importance: Lesioning procedures are effective for trigeminal neuralgia (TN), but late pain recurrence associated with sensory recovery is common. We report a case of recurrence of type 1A TN and recovery of facial sensory function after trigeminal rhizotomy associated with collateral sprouting from upper cervical spinal nerves.

Clinical Presentation: A 41-yr-old woman presented 2 yr after open left trigeminal sensory rhizotomy for TN with pain-free anesthesia in the entire left trigeminal nerve distribution. Over 18 mo, she developed gradual recovery of facial sensation migrating anteromedially from the occipital region, eventually extending to the midpupillary line across the distribution of all trigeminal nerve branches. She reported recurrence of her triggered lancinating TN pain isolated to the area of recovered sensation with no pain in anesthetic areas. Nerve ultrasound demonstrated enlargement of ipsilateral greater and lesser occipital nerves, and occipital nerve block restored facial anesthesia and resolved her pain, indicating that recovered facial sensation was provided exclusively by the upper cervical spinal nerves. She underwent C2/C3 ganglionectomy, and ganglia were observed to be hypertrophic. Postoperatively, trigeminal anesthesia was restored with complete resolution of pain that persisted at 12-mo follow-up.

Conclusion: This is the first documented case of a spinal nerve innervating a cranial dermatome by collateral sprouting after cranial nerve injury. The fact that typical TN pain can occur even when sensation is mediated by spinal nerves suggests that the disorder can be centrally mediated and late failure after lesioning procedures may result from maladaptive reinnervation.
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http://dx.doi.org/10.1093/neuros/nyz306DOI Listing
May 2020

Commentary: The Emerging Role of Biomarkers in Adaptive Modulation of Clinical Brain Stimulation.

Neurosurgery 2019 09;85(3):E440-E441

Case Western Reserve, University School of Medicine, Cleveland, Ohio.

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http://dx.doi.org/10.1093/neuros/nyz097DOI Listing
September 2019

Clinical Evaluation of Cingulum Bundle Connectivity for Neurosurgical Hypothesis Development.

Neurosurgery 2020 05;86(5):724-735

Case Western Reserve University, Cleveland, Ohio.

Background: The cingulum bundle (CB) has long been a target for psychiatric neurosurgical procedures, but with limited understanding of the brain networks being impacted. Recent advances in human tractography could provide a foundation to better understand the effects of neurosurgical interventions on the CB; however, the reliability of tractography remains in question.

Objective: To evaluate the ability of different tractography techniques, derived from typical, human diffusion-weighted imaging (DWI) data, to characterize CB connectivity described in animal models. This will help validate the clinical applicability of tractography, and generate insight on current and future neurosurgical targets for psychiatric disorders.

Methods: Connectivity of the CB in 15 healthy human subjects was evaluated using DWI-based tractography, and compared to tract-tracing findings from nonhuman primates. Brain regions of interest were defined to coincide with the animal model. Tractography was performed using 3 techniques (FSL probabilistic, Camino probabilistic, and Camino deterministic). Differences in connectivity were assessed, and the CB segment with the greatest connectivity was determined.

Results: Each tractography technique successfully reproduced the animal tracing model with a mean accuracy of 72% (68-75%, P < .05). Additionally, one region of the CB, the rostral dorsal segment, had significantly greater connectivity to associated brain structures than all other CB segments (P < .05).

Conclusion: Noninvasive, in vivo human analysis of the CB, using clinically available DWI for tractography, consistently reproduced the results of an animal tract-tracing model. This suggests that tractography of the CB can be used for clinical applications, which may aid in neurosurgical targeting for psychiatric disorders.
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http://dx.doi.org/10.1093/neuros/nyz225DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7156292PMC
May 2020

Principled BCI Decoder Design and Parameter Selection Using a Feedback Control Model.

Sci Rep 2019 06 20;9(1):8881. Epub 2019 Jun 20.

Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio, USA.

Decoders optimized offline to reconstruct intended movements from neural recordings sometimes fail to achieve optimal performance online when they are used in closed-loop as part of an intracortical brain-computer interface (iBCI). This is because typical decoder calibration routines do not model the emergent interactions between the decoder, the user, and the task parameters (e.g. target size). Here, we investigated the feasibility of simulating online performance to better guide decoder parameter selection and design. Three participants in the BrainGate2 pilot clinical trial controlled a computer cursor using a linear velocity decoder under different gain (speed scaling) and temporal smoothing parameters and acquired targets with different radii and distances. We show that a user-specific iBCI feedback control model can predict how performance changes under these different decoder and task parameters in held-out data. We also used the model to optimize a nonlinear speed scaling function for the decoder. When used online with two participants, it increased the dynamic range of decoded speeds and decreased the time taken to acquire targets (compared to an optimized standard decoder). These results suggest that it is feasible to simulate iBCI performance accurately enough to be useful for quantitative decoder optimization and design.
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http://dx.doi.org/10.1038/s41598-019-44166-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6586941PMC
June 2019

(-)-Phenserine Ameliorates Contusion Volume, Neuroinflammation, and Behavioral Impairments Induced by Traumatic Brain Injury in Mice.

Cell Transplant 2019 Sep-Oct;28(9-10):1183-1196. Epub 2019 Jun 10.

The Ph.D. Program for Neural Regenerative Medicine, College of Medical Science and Technology, Taipei Medical University, Taipei.

Traumatic brain injury (TBI), a major cause of mortality and morbidity, affects 10 million people worldwide, with limited treatment options. We have previously shown that (-)-phenserine (Phen), an acetylcholinesterase inhibitor originally designed and tested in clinical phase III trials for Alzheimer's disease, can reduce neurodegeneration after TBI and reduce cognitive impairments induced by mild TBI. In this study, we used a mouse model of moderate to severe TBI by controlled cortical impact to assess the effects of Phen on post-trauma histochemical and behavioral changes. Animals were treated with Phen (2.5 mg/kg, IP, BID) for 5 days started on the day of injury and the effects were evaluated by behavioral and histological examinations at 1 and 2 weeks after injury. Phen significantly attenuated TBI-induced contusion volume, enlargement of the lateral ventricle, and behavioral impairments in motor asymmetry, sensorimotor functions, motor coordination, and balance functions. The morphology of microglia was shifted to an active from a resting form after TBI, and Phen dramatically reduced the ratio of activated to resting microglia, suggesting that Phen also mitigates neuroinflammation after TBI. While Phen has potent anti-acetylcholinesterase activity, its (+) isomer Posiphen shares many neuroprotective properties but is almost completely devoid of anti-acetylcholinesterase activity. We evaluated Posiphen at a similar dose to Phen and found similar mitigation in lateral ventricular size increase, motor asymmetry, motor coordination, and balance function, suggesting the improvement of these histological and behavioral tests by Phen treatment occur via pathways other than anti-acetylcholinesterase inhibition. However, the reduction of lesion size and improvement of sensorimotor function by Posiphen were much smaller than with equivalent doses of Phen. Taken together, these results show that post-injury treatment with Phen over 5 days significantly ameliorates severity of TBI. These data suggest a potential development of this compound for clinical use in TBI therapy.
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http://dx.doi.org/10.1177/0963689719854693DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6767878PMC
August 2020

Potential Deep Brain Stimulation Targets for the Management of Refractory Hypertension.

Front Neurosci 2019 25;13:93. Epub 2019 Feb 25.

Department of Neurological Surgery, Neurological Institute, University Hospitals Cleveland Medical Center, Cleveland, OH, United States.

Hypertension is the single greatest contributor to human disease and mortality affecting over 75 million people in the United States alone. Hypertension is defined according to the American College of Cardiology as systolic blood pressure (SBP) greater than 120 mm Hg and diastolic blood pressure (DBP) above 80 mm Hg measured on two separate occasions. While there are multiple medication classes available for blood pressure control, fewer than 50% of hypertensive patients maintain appropriate control. In fact, 0.5% of patients are refractory to medical treatment which is defined as uncontrolled blood pressure despite treatment with five classes of antihypertensive agents. With new guidelines to define hypertension that will increase the incidence of hypertension world-wide, the prevalence of refractory hypertension is expected to increase. Thus, investigation into alternative methods of blood pressure control will be crucial to reduce comorbidities such as higher risk of myocardial infarction, cardiovascular accident, aneurysm formation, heart failure, coronary artery disease, end stage renal disease, arrhythmia, left ventricular hypertrophy, intracerebral hemorrhage, hypertensive enchaphelopathy, hypertensive retinopathy, glomerulosclerosis, limb loss due to arterial occlusion, and sudden death. Recently, studies demonstrated efficacious treatment of neurological diseases with deep brain stimulation (DBS) for Tourette's, depression, intermittent explosive disorder, epilepsy, chronic pain, and headache as these diseases have defined neurophysiology with anatomical targets. Currently, clinical applications of DBS is limited to neurological conditions as such conditions have well-defined neurophysiology and anatomy. However, rapidly expanding knowledge about neuroanatomical controls of systemic conditions such as hypertension are expanding the possibilities for DBS neuromodulation. Within the central autonomic network (CAN), multiple regions play a role in homeostasis and blood pressure control that could be DBS targets. While the best defined autonomic target is the ventrolateral periaqueductal gray matter, other targets including the subcallosal neocortex, subthalamic nucleus (STN), posterior hypothalamus, rostrocaudal cingulate gyrus, orbitofrontal gyrus, and insular cortex are being further characterized as potential targets. This review aims to summarize the current knowledge regarding neurologic contribution to the pathophysiology of hypertension, delineate the complex interactions between neuroanatomic structures involved in blood pressure homeostasis, and then discuss the potential for using DBS as a treatment for refractory hypertension.
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http://dx.doi.org/10.3389/fnins.2019.00093DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6397890PMC
February 2019

Evolution in the Treatment of Psychiatric Disorders: From Psychosurgery to Psychopharmacology to Neuromodulation.

Front Neurosci 2019 15;13:108. Epub 2019 Feb 15.

Department of Neurosurgery, University Hospitals Cleveland Medical Center, Case Western Reserve University, Cleveland, OH, United States.

The treatment of psychiatric patients presents significant challenges to the clinical community, and a multidisciplinary approach to diagnosis and management is essential to facilitate optimal care. In particular, the neurosurgical treatment of psychiatric disorders, or "psychosurgery," has held fascination throughout human history as a potential method of influencing behavior and consciousness. Early evidence of such procedures can be traced to prehistory, and interest flourished in the nineteenth and early twentieth century with greater insight into cerebral functional and anatomic localization. However, any discussion of psychosurgery invariably invokes controversy, as the widespread and indiscriminate use of the transorbital lobotomy in the mid-twentieth century resulted in profound ethical ramifications that persist to this day. The concurrent development of effective psychopharmacological treatments virtually eliminated the need and desire for psychosurgical procedures, and accordingly the research and practice of psychosurgery was dormant, but not forgotten. There has been a recent resurgence of interest for non-ablative therapies, due in part to modern advances in functional and structural neuroimaging and neuromodulation technology. In particular, deep brain stimulation is a promising treatment paradigm with the potential to modulate abnormal pathways and networks implicated in psychiatric disease states. Although there is enthusiasm regarding these recent advancements, it is important to reflect on the scientific, social, and ethical considerations of this controversial field.
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http://dx.doi.org/10.3389/fnins.2019.00108DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6384258PMC
February 2019

Classification of paroxysmal events and the four-dimensional epilepsy classification system.

Epileptic Disord 2019 02;21(1):1-29

Case Medical Center - Pediatrics, Cleveland, Ohio, USA.

This educational review describes the classification of paroxysmal events and a four-dimensional epilepsy classification system. Paroxysmal events are classified as epileptic and non-epileptic paroxysmal events. Non-epileptic events are, in turn, classified as psychogenic and organic paroxysmal events. The following four dimensions are used to classify epileptic paroxysmal events: ictal semiology, the epileptogenic zone, etiology, and comorbidities. Efforts are made to keep these four dimensions as independent as possible. The review also includes 12 educational vignettes and three more detailed case reports classified using the 2017 classification of the ILAE and the four-dimensional epilepsy classification. In addition, a case is described which is classified using the four-dimensional epilepsy classification with different degrees of precision by an emergency department physician, a neurologist, and an epileptologist. [Published with video sequences on www.epilepticdisorders.com].
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http://dx.doi.org/10.1684/epd.2019.1033DOI Listing
February 2019

Post-Injury Neuroprotective Effects of the Thalidomide Analog 3,6'-Dithiothalidomide on Traumatic Brain Injury.

Int J Mol Sci 2019 Jan 24;20(3). Epub 2019 Jan 24.

Graduate Institute of Medical Sciences, College of Medicine, Taipei Medical University, 250 Wu-Xing Street, Taipei 11031, Taiwan.

Traumatic brain injury (TBI) is a major cause of mortality and disability worldwide. Long-term deficits after TBI arise not only from the direct effects of the injury but also from ongoing processes such as neuronal excitotoxicity, inflammation, oxidative stress and apoptosis. Tumor necrosis factor-α (TNF-α) is known to contribute to these processes. We have previously shown that 3,6'-dithiothalidomide (3,6'-DT), a thalidomide analog that is more potent than thalidomide with similar brain penetration, selectively inhibits the synthesis of TNF-α in cultured cells and reverses behavioral impairments induced by mild TBI in mice. In the present study, we further explored the therapeutic potential of 3,6'-DT in an animal model of moderate TBI using Sprague-Dawley rats subjected to controlled cortical impact. A single dose of 3,6'-DT (28 mg/kg, i.p.) at 5 h after TBI significantly reduced contusion volume, neuronal degeneration, neuronal apoptosis and neurological deficits at 24 h post-injury. Expression of pro-inflammatory cytokines in the contusion regions were also suppressed at the transcription and translation level by 3,6'-DT. Notably, neuronal oxidative stress was also suppressed by 3,6'-DT. We conclude that 3,6'-DT may represent a potential therapy to ameliorate TBI-induced functional deficits.
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http://dx.doi.org/10.3390/ijms20030502DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6387371PMC
January 2019

Limbic and paralimbic structures driving ictal central apnea.

Neurology 2019 02 11;92(7):e655-e669. Epub 2019 Jan 11.

From the Epilepsy Center (N.L., J.P.H., J.P.M., S.L.), University Hospitals Cleveland Medical Center, OH; Department of Neurobiology and the Brain Research Institute (R.M.H.), University of California, Los Angeles; and NINDS Center for SUDEP Research (R.M.H., S.L.), Case Western Reserve University, Cleveland, OH.

Objective: To precisely identify cortical regions that modulate breathing, and delineate a network of cortical structures that underpin ictal central apnea (ICA) during epileptic seizures.

Methods: We electrically stimulated multiple cortical structures in patients undergoing stereotactic EEG (SEEG) evaluation before epilepsy surgery. Structures investigated were orbitofrontal cortex, anterior and posterior cingulate and subcallosal gyri, insula, hippocampus, parahippocampal gyrus, amygdala, temporo-polar cortex, antero-mesial fusiform gyrus, and lateral and basal temporal cortices. Chest/abdominal excursions using thoracic/abdominal belts, peripheral capillary oxygen saturation, end tidal and transcutaneous carbon dioxide, and airflow were continuously monitored.

Results: Nineteen consecutive adult patients (10 female) aged 18-69 years were investigated. Transient central apnea was elicited in 13/19 patients with amygdala, hippocampus head and body, anterior parahippocampal gyrus, and antero-mesial fusiform gyrus. Insula, cingulate, subcallosal, orbitofrontal, lateral, and basal temporal cortices stimulation did not induce apnea. Apnea duration was associated with stimulus duration ( < 0.001) and current intensity ( = 0.004).

Conclusions: These findings suggest a limbic/paralimbic mesial temporal breathing modulation network that includes amygdala, hippocampus, anterior parahippocampal, and antero-mesial fusiform gyri. These structures likely represent anatomical and functional substrates for ICA, a putative sudden unexpected death in epilepsy (SUDEP) breathing biomarker. Damage to such areas is known to occur in high SUDEP risk patients and SUDEP victims, and may underpin the prolonged ICA that is thought to be particularly dangerous. Furthermore, inclusive targeting of apnea-producing structures in SEEG implantations, peri-ictal breathing signal recordings, and stringent analysis of apneic sequences in seizure semiology may enhance accurate identification of symptomatogenic and seizure onset zones for epilepsy surgery.
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http://dx.doi.org/10.1212/WNL.0000000000006920DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6382368PMC
February 2019

Surgery for epilepsy in the primary motor cortex: A critical review.

Epilepsy Behav 2019 02 23;91:13-19. Epub 2018 Jul 23.

Department of Neurosurgery, University Hospitals Cleveland Medical Center, Case Western Reserve University, Cleveland, OH, USA. Electronic address:

Surgical resection of the epileptogenic zone within the frontal lobe can be a very effective treatment for medically refractory epilepsy originating from this area. While much of the frontal lobe consists of highly eloquent tissue, surgery is not necessarily contraindicated as long as the epileptogenic zone is well-localized and the tissue resected is limited. Resection of the primary motor cortex was described by Victor Horsley in the 19th century and was used frequently in the early 20th century for a variety of neurological disorders including epilepsy; improvements in surgical techniques and mapping has led to a resurgence of its use in the past few decades. Although many surgeons are hesitant to resect tissue adjacent to the primary hand area based on fears of new motor deficits, there is extensive evidence that focal resections are well-tolerated over the long-term with residual weakness that is fairly mild: some patients experience postoperative weakness, including hemiparesis, but a stereotypical recovery of strength from proximal to distal muscles occurs over months, and only one quarter will have a permanent neurologic deficit, usually consisting of difficulty with fine motor movements. The main alternative to surgical resection is subpial transection, characterized by a small decrease in postoperative deficits and significantly worse seizure outcomes. The treatment of patients with seizures originating from this region requires a solid understanding of the structural and functional anatomy of the frontal lobe.
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http://dx.doi.org/10.1016/j.yebeh.2018.06.036DOI Listing
February 2019

A Comparison of Intention Estimation Methods for Decoder Calibration in Intracortical Brain-Computer Interfaces.

IEEE Trans Biomed Eng 2018 09 14;65(9):2066-2078. Epub 2017 Dec 14.

Objective: Recent reports indicate that making better assumptions about the user's intended movement can improve the accuracy of decoder calibration for intracortical brain-computer interfaces. Several methods now exist for estimating user intent, including an optimal feedback control model, a piecewise-linear feedback control model, ReFIT, and other heuristics. Which of these methods yields the best decoding performance?

Methods: Using data from the BrainGate2 pilot clinical trial, we measured how a steady-state velocity Kalman filter decoder was affected by the choice of intention estimation method. We examined three separate components of the Kalman filter: dimensionality reduction, temporal smoothing, and output gain (speed scaling).

Results: The decoder's dimensionality reduction properties were largely unaffected by the intention estimation method. Decoded velocity vectors differed by <5% in terms of angular error and speed vs. target distance curves across methods. In contrast, the smoothing and gain properties of the decoder were greatly affected (> 50% difference in average values). Since the optimal gain and smoothing properties are task-specific (e.g. lower gains are better for smaller targets but worse for larger targets), no one method was better for all tasks.

Conclusion: Our results show that, when gain and smoothing differences are accounted for, current intention estimation methods yield nearly equivalent decoders and that simple models of user intent, such as a position error vector (target position minus cursor position), perform comparably to more elaborate models. Our results also highlight that simple differences in gain and smoothing properties have a large effect on online performance and can confound decoder comparisons.
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http://dx.doi.org/10.1109/TBME.2017.2783358DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6043406PMC
September 2018

Noninvasive Presurgical Data for One-Stage Leucotomy in Catastrophic Epilepsy.

World Neurosurg 2018 Aug 1;116:268-273. Epub 2018 Jun 1.

Department of Neurosurgery, Neurological Institute, University Hospitals of Cleveland Medical Center, Cleveland, Ohio, USA; Case Western Reserve University School of Medicine, Cleveland, Ohio, USA.

Background: Catastrophic epilepsy results in severe neurodevelopmental delay in infants because of frequent and/or long seizures. Therefore, consideration of early epilepsy surgery is essential for neurodevelopmental outcome. Once an infant with catastrophic seizures is identified as a surgical candidate, it is important that the surgical plan be carefully defined based on detailed presurgical evidence to minimize surgical complications in this age group.

Case Description: We present 2 infants with catastrophic epilepsy, epileptic spasms, and bihemispheric electroencephalographic abnormalities who underwent one-stage disconnection surgery based on a sound hypothesis of the epileptogenic zone. Each patient underwent an extensive noninvasive presurgical investigation followed by stereotactic disconnection leucotomy in a single stage. After the 2 children were followed for 24-36 months. A seizure reduction by at least 90% (Engel class I) was achieved in both cases with subsequent improvement in neurodevelopmental progress. There were no perioperative complications. Both patients had widespread cortical dysplasia on pathologic evaluation.

Conclusions: Careful consideration of the noninvasive presurgical workup can identify focal onset even in the presence of catastrophic epilepsy with widespread bilateral abnormalities. Single-stage lobar leucotomy for disconnection of the epileptogenic zone can lead to excellent outcome in these patients.
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http://dx.doi.org/10.1016/j.wneu.2018.05.182DOI Listing
August 2018

Toward Functional Restoration of the Central Nervous System: A Review of Translational Neuroscience Principles.

Neurosurgery 2019 01;84(1):30-40

Department of Neurosurgery, Duke University Medical Center, Durham, North Carolina.

Injury to the central nervous system (CNS) can leave patients with devastating neurological deficits that may permanently impair independence and diminish quality of life. Recent insights into how the CNS responds to injury and reacts to critically timed interventions are being translated into clinical applications that have the capacity to drastically improve outcomes for patients suffering from permanent neurological deficits due to spinal cord injury, stroke, or other CNS disorders. The translation of such knowledge into practical and impactful treatments involves the strategic collaboration between neurosurgeons, clinicians, therapists, scientists, and industry. Therefore, a common understanding of key neuroscientific principles is crucial. Conceptually, current approaches to CNS revitalization can be divided by scale into macroscopic (systems-circuitry) and microscopic (cellular-molecular). Here we review both emerging and well-established tenets that are being utilized to enhance CNS recovery on both levels, and we explore the role of neurosurgeons in developing therapies moving forward. Key principles include plasticity-driven functional recovery, cellular signaling mechanisms in axonal sprouting, critical timing for recovery after injury, and mechanisms of action underlying cellular replacement strategies. We then discuss integrative approaches aimed at synergizing interventions across scales, and we make recommendations for the basis of future clinical trial design. Ultimately, we argue that strategic modulation of microscopic cellular behavior within a macroscopic framework of functional circuitry re-establishment should provide the foundation for most neural restoration strategies, and the early involvement of neurosurgeons in the process will be crucial to successful clinical translation.
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http://dx.doi.org/10.1093/neuros/nyy128DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6292792PMC
January 2019

Profound deficits in hippocampal synaptic plasticity after traumatic brain injury and seizure is ameliorated by prophylactic levetiracetam.

Oncotarget 2018 Feb 4;9(14):11515-11527. Epub 2018 Jan 4.

Department of Neurosurgery, Case Western Reserve University School of Medicine, Cleveland, Ohio, USA.

Aim: To determine the precise effects of post-traumatic seizure activity on hippocampal processes, we induced seizures at various intervals after traumatic brain injury (TBI) and analyzed plasticity at CA1 Schaffer collateral synapses.

Material And Methods: Rats were initially separated into two groups; one exposed solely to fluid percussion injury (FPI) at 2 Psi and the other only receiving kainic acid (KA)-induced seizures without FPI. Electrophysiological (ePhys) studies including paired-pulse stimulation for short-term presynaptic plasticity and long-term potentiation (LTP) of CA1 Schaffer collateral synapses of the hippocampus for post-synaptic function survey were followed at post-event 1 hour, 3 and 7 days respectively. Additional rats were exposed to three seizures at weekly intervals starting 1 week or 2 weeks after TBI and compared with seizures without TBI, TBI without seizures, and uninjured animals. An additional group placed under the same control variables were treated with levetiracetam prior to seizure induction. The ePhys studies related to post-TBI induced seizures were also followed in these additional groups.

Results: Seizures affected the short- and long-term synaptic plasticity of the hippocampal CA3-CA1 pathway. FPI itself suppressed LTP and field excitatory post synaptic potentials (fEPSP) in the CA1 Schaffer collateral synapses; KA-induced seizures that followed FPI further suppressed synaptic plasticity. The impairments in both short-term presynaptic and long-term plasticity were worse in the rats in which early post-TBI seizures were induced than those in which later post-TBI seizures were induced. Finally, prophylactic infusion of levetiracetam for one week after FPI reduced the synaptic plasticity deficits in early post-TBI seizure animals.

Conclusion: Our data indicates that synaptic plasticity (i.e., both presynaptic and postsynaptic) suppression occurs in TBI followed by a seizure and that the interval between the TBI and seizure is an important factor in the severity of the resulting deficits. Furthermore, the infusion of prophylactic levetiracetam could partially reverse the suppression of synaptic plasticity.
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http://dx.doi.org/10.18632/oncotarget.23923DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5837755PMC
February 2018

Radiofrequency Energy and Electrode Proximity Influences Stereoelectroencephalography-Guided Radiofrequency Thermocoagulation Lesion Size: An In Vitro Study with Clinical Correlation.

Oper Neurosurg (Hagerstown) 2018 10;15(4):461-469

Department of Neurosurgery, University Hospital Cleveland Medical Center, Case Western Reserve University School of Medicine, Cleveland, Ohio.

Background: Radiofrequency thermocoagulation of epileptogenic foci via stereoelectroencephalography (SEEG) electrodes has been suggested as a treatment for medically intractable epilepsy, but reported outcomes have been suboptimal, possibly because lesions generated using conventional high-energy radiofrequency parameters are relatively small.

Objective: To describe a technique of delivering low energy across separate SEEG electrodes in order to create large confluent radiofrequency lesions.

Methods: The size and configuration of radiofrequency lesions using different radiofrequency intensity and interelectrode distance was assessed in egg whites. Magnetic resonance images (MRI) from 3 patients who had undergone radiofrequency lesion creation were evaluated to determine the contribution of lesion intensity and electrode separation on lesion size. Electroencephalography, MRI, and clinical data were assessed before and after lesion creation.

Results: Both in Vitro and in Vivo analysis revealed that less energy paradoxically produced larger lesions, with the largest possible lesions produced when radiofrequency power was applied for long duration at less than 3 W. Linear separation of electrodes also contributed to lesion size, with largest lesions produced when electrodes were separated by a linear distance of between 5 and 12 mm. Clinical lesions produced using these parameters were large and resulted in improvement in interictal and ictal activity.

Conclusion: Radiofrequency lesions produced using low-energy delivery between SEEG electrodes in close proximity can produce a large lesion. These findings might have advantages for treatment of focal epilepsy.
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http://dx.doi.org/10.1093/ons/opx291DOI Listing
October 2018

Charting the road forward in psychiatric neurosurgery: proceedings of the 2016 American Society for Stereotactic and Functional Neurosurgery workshop on neuromodulation for psychiatric disorders.

J Neurol Neurosurg Psychiatry 2018 08 25;89(8):886-896. Epub 2018 Jan 25.

Department of Neurosurgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA.

Objective: Refractory psychiatric disease is a major cause of morbidity and mortality worldwide, and there is a great need for new treatments. In the last decade, investigators piloted novel deep brain stimulation (DBS)-based therapies for depression and obsessive-compulsive disorder (OCD). Results from recent pivotal trials of these therapies, however, did not demonstrate the degree of efficacy expected from previous smaller trials. To discuss next steps, neurosurgeons, neurologists, psychiatrists and representatives from industry convened a workshop sponsored by the American Society for Stereotactic and Functional Neurosurgery in Chicago, Illinois, in June of 2016.

Design: Here we summarise the proceedings of the workshop. Participants discussed a number of issues of importance to the community. First, we discussed how to interpret results from the recent pivotal trials of DBS for OCD and depression. We then reviewed what can be learnt from lesions and closed-loop neurostimulation. Subsequently, representatives from the National Institutes of Health, the Food and Drug Administration and industry discussed their views on neuromodulation for psychiatric disorders. In particular, these third parties discussed their criteria for moving forward with new trials. Finally, we discussed the best way of confirming safety and efficacy of these therapies, including registries and clinical trial design. We close by discussing next steps in the journey to new neuromodulatory therapies for these devastating illnesses.

Conclusion: Interest and motivation remain strong for deep brain stimulation for psychiatric disease. Progress will require coordinated efforts by all stakeholders.
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http://dx.doi.org/10.1136/jnnp-2017-317082DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7340367PMC
August 2018

Rapid calibration of an intracortical brain-computer interface for people with tetraplegia.

J Neural Eng 2018 04;15(2):026007

Neuroscience Graduate Program, Brown University, Providence, RI, United States of America. Department of Neuroscience, Brown University, Providence, RI, United States of America. Brown Institute for Brain Science, Brown University, Providence, RI, United States of America. Department of Surgery (Neurosurgery), Dalhousie University, Halifax, NS, Canada.

Objective: Brain-computer interfaces (BCIs) can enable individuals with tetraplegia to communicate and control external devices. Though much progress has been made in improving the speed and robustness of neural control provided by intracortical BCIs, little research has been devoted to minimizing the amount of time spent on decoder calibration.

Approach: We investigated the amount of time users needed to calibrate decoders and achieve performance saturation using two markedly different decoding algorithms: the steady-state Kalman filter, and a novel technique using Gaussian process regression (GP-DKF).

Main Results: Three people with tetraplegia gained rapid closed-loop neural cursor control and peak, plateaued decoder performance within 3 min of initializing calibration. We also show that a BCI-naïve user (T5) was able to rapidly attain closed-loop neural cursor control with the GP-DKF using self-selected movement imagery on his first-ever day of closed-loop BCI use, acquiring a target 37 s after initiating calibration.

Significance: These results demonstrate the potential for an intracortical BCI to be used immediately after deployment by people with paralysis, without the need for user learning or extensive system calibration.
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http://dx.doi.org/10.1088/1741-2552/aa9ee7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5823702PMC
April 2018

A novel use of the NeuroBlate SideFire probe for minimally invasive disconnection of a hypothalamic hamartoma in a child with gelastic seizures.

J Neurosurg Pediatr 2018 03 12;21(3):302-307. Epub 2018 Jan 12.

1Department of Neurological Surgery, University Hospitals, Case Western Reserve University.

The authors describe the case of a 22-month-old boy who presented with gelastic seizures and developmental delay. Magnetic resonance imaging and video-electroencephalography monitoring revealed a primarily intraventricular hypothalamic hamartoma and gelastic seizures occurring 20-30 times daily. The patient was treated with various regimens of antiepileptic medications for 16 months, but the seizures remained medically intractable. At 3 years of age, he underwent stereotactic laser ablation with an aim of disconnection of the lesion. The procedure was performed with the NeuroBlate SideFire probe. To the authors' knowledge, this is the first reported use of this technology for this procedure and serves as proof of concept. There were no perioperative complications, and 2 years postprocedure, the patient remains seizure free with marked behavioral and cognitive improvements.
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http://dx.doi.org/10.3171/2017.9.PEDS1747DOI Listing
March 2018

Implementation of a "Flipped Classroom" for Neurosurgery Resident Education.

Can J Neurol Sci 2018 01 18;45(1):76-82. Epub 2017 Sep 18.

Department of Neurosurgery,University Hospitals Cleveland Medical Center,Cleveland,Ohio,USA.

Introduction: Engaging residents across a multiyear training spectrum is challenging given the heterogeneity of experience and limited time available for educational activities. A "flipped classroom" model, in which residents prepare ahead of time for mentored topic discussions, has potential advantages.

Methods: We implemented a curriculum consisting of topics distributed across the specialty. Weekly, each resident was randomly assigned to research a specific aspect of an assigned topic appropriate to his or her level of experience: junior residents about what characterizes each clinical entity, midlevel residents about when to intervene, and chief residents about how to administer treatment. Residents completed an anonymous survey 6 months after implementation. Board examination performance was assessed before and after implementation.

Results: A total of 12 residents participated in the program. Weekly, 1.75±0.40 hours were spent in preparation, with senior residents reporting less time than junior residents. All residents indicated that the accumulation of experience across 7 years of residency was a major advantage of this program, and all preferred it to lectures. Performance on the board examination significantly increased after implementation (from 316±36 to 468±45, p<0.05).

Conclusions: The flipped classroom is a viable approach to resident education and is associated with increased engagement and improved performance using validated knowledge-assessment tools.
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http://dx.doi.org/10.1017/cjn.2017.234DOI Listing
January 2018

Surgical Management of Deep Brain Stimulator Scalp Erosion without Hardware Removal.

Stereotact Funct Neurosurg 2017 13;95(6):385-391. Epub 2017 Dec 13.

Department of Neurosurgery, University Hospitals Cleveland Medical Center, Case Western Reserve University, Cleveland, OH, USA.

Background: Scalp erosion in patients with deep brain stimulation (DBS) hardware is an uncommon complication that lacks a clearly defined management strategy. Previous studies have described various therapies including conservative treatment with antibiotics and surgical debridement with or without hardware removal.

Objectives: The aim of this study was to review the efficacy of a hardware-sparing management strategy for the treatment of scalp erosion.

Methods: Five patients with previous DBS implantation presented with scalp erosion and visible hardware exposure at the calvarial burr hole site, and underwent tension-free, vascularized, rotational scalp flap, with preservation of the leads under the pericranium. Two of the procedures were performed after an unsuccessful attempt at primary closure and 3 as a primary procedure. Each patient was followed clinically for at least 14 months postoperatively to evaluate for wound-healing and adverse effects.

Results: The median duration from initial DBS hardware implantation to erosion and revision surgery was 12 months (range 1.5-62 months). Three patients were documented to have positive intraoperative cultures in spite of the absence of purulence. At the last follow-up, all patients were noted to have complete wound-healing and no evidence of infection or erosion.

Conclusions: DBS scalp erosion can be managed by rotational scalp flap without hardware removal, even in cases where infection is identified.
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http://dx.doi.org/10.1159/000484323DOI Listing
December 2018

Resection of Temporal Neocortex During Multiple Hippocampal Transections for Mesial Temporal Lobe Epilepsy Does not Affect Seizure or Memory Outcome.

Oper Neurosurg (Hagerstown) 2017 12;13(6):711-717

Department of Neurosurgery, University Hospital Case Medical Center, Case Western Reserve University School of Medicine, Cleveland, Ohio.

Background: Multiple hippocampal transection (MHT) is a surgical treatment for mesial temporal lobe epilepsy associated with improved postoperative neuropsychological outcomes compared with lobectomy.

Objective: To determine whether resection of the amygdala and anterior temporal neocortex during MHT affects postoperative seizure/memory outcome.

Methods: Seventeen patients with normal magnetic resonance imaging and stereo-electroencephalogram-proven drug-resistant dominant mesial temporal lobe epilepsy were treated with MHT. Nine patients underwent MHT alone (MHT-) and 8 patients underwent MHT plus removal of the amygdala and anterior 4.5 cm of temporal neocortex lateral to the fusiform gyrus (MHT+). Verbal and visual-spatial memory were assessed in all patients preoperatively and in 14 patients postoperatively using the Wechsler Memory Scale. Postoperative seizure control was assessed at 12 months for all patients.

Results: Overall, 11 of 17 patients (64.7%) were Engel class 1 at 1 year (6/9 MHT-, 5/8 MHT+, P = .38), and 10 of 14 patients (71.4%) had no significant postoperative decline in either verbal or visual memory (6/8 MHT-, 4/6 MHT+, P = .42). Verbal memory declined in 2 of 8 MHT- and 1 of 6 MHT+ patients, and visual memory declined in 1 of 8 MHT- and 2 of 6 MHT+ patients. Two patients had improved visual memory postoperatively, both in the MHT+ group.

Conclusion: MHT on the dominant side is associated with high rates of seizure freedom and favorable memory preservation outcomes regardless of the extent of neocortical resection. Preservation of the temporal neocortex and amygdala during MHT does not appear to decrease the risk of postoperative memory decline, nor does it alter seizure outcome.
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http://dx.doi.org/10.1093/ons/opx031DOI Listing
December 2017

Cortical Structures Associated With Human Blood Pressure Control.

JAMA Neurol 2018 02;75(2):194-202

Epilepsy Center, University Hospitals Cleveland Medical Center, Cleveland, Ohio.

Importance: A better understanding of the role of cortical structures in blood pressure control may help us understand cardiovascular collapse that may lead to sudden unexpected death in epilepsy (SUDEP).

Objective: To identify cortical control sites for human blood pressure regulation.

Design, Setting, And Participants: Patients with intractable epilepsy undergoing intracranial electrode implantation as a prelude to epilepsy surgery in the Epilepsy Monitoring Unit at University Hospitals Cleveland Medical Center were potential candidates for this study. Inclusion criteria were patients 18 years or older who had electrodes implanted in one or more of the regions of interest and in whom deep brain electrical stimulation was indicated for mapping of ictal onset or eloquent cortex as a part of the presurgical evaluation. Twelve consecutive patients were included in this prospective case series from June 1, 2015, to February 28, 2017.

Main Outcomes And Measures: Changes in continuous, noninvasive, beat-by-beat blood pressure parameter responses from amygdala, hippocampal, insular, orbitofrontal, temporal, cingulate, and subcallosal stimulation. Electrocardiogram, arterial oxygen saturation, end-tidal carbon dioxide, nasal airflow, and abdominal and thoracic plethysmography were monitored.

Results: Among 12 patients (7 female; mean [SD] age, 44.25 [12.55] years), 9 electrodes (7 left and 2 right) all in Brodmann area 25 (subcallosal neocortex) in 4 patients produced striking systolic hypotensive changes. Well-maintained diastolic arterial blood pressure and narrowed pulse pressure indicated stimulation-induced reduction in sympathetic drive and consequent probable reduction in cardiac output rather than bradycardia or peripheral vasodilation-induced hypotension. Frequency-domain analysis of heart rate and blood pressure variability showed a mixed picture. No other stimulated structure produced significant blood pressure changes.

Conclusions And Relevance: These findings suggest that Brodmann area 25 has a role in lowering systolic blood pressure in humans. It is a potential symptomatogenic zone for peri-ictal hypotension in patients with epilepsy.
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http://dx.doi.org/10.1001/jamaneurol.2017.3344DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5838633PMC
February 2018
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