Hippocampal CA1 and CA3 neural recording in the human brain: validation of depth electrode placement through high-resolution imaging and electrophysiology

OBJECTIVEIntracranial human brain recordings typically utilize recording systems that do not distinguish individual neuron action potentials. In such cases, individual neurons are not identified by location within functional circuits. In this paper, verified localization of singly recorded hippocampal neurons within the CA3 and CA1 cell fields is demonstrated.METHODSMacro-micro depth electrodes were implanted in 23 human patients undergoing invasive monitoring for identification of epileptic seizure foci. Individual neurons were isolated and identified via extracellular action potential waveforms recorded via macro-micro depth electrodes localized within the hippocampus. A morphometric survey was performed using 3T MRI scans of hippocampi from the 23 implanted patients, as well as 46 normal (i.e., nonepileptic) patients and 26 patients with a history of epilepsy but no history of depth electrode placement, which provided average dimensions of the hippocampus along typical implantation tracks. Localization within CA3 and CA1 cell fields was tentatively assigned on the basis of recording electrode site, stereotactic positioning of the depth electrode in comparison with the morphometric survey, and postsurgical MRI. Cells were selected as candidate CA3 and CA1 principal neurons on the basis of waveform and firing rate characteristics and confirmed within the CA3-to-CA1 neural projection pathways via measures of functional connectivity.RESULTSCross-correlation analysis confirmed that nearly 80% of putative CA3-to-CA1 cell pairs exhibited positive correlations compatible with feed-forward connection between the cells, while only 2.6% exhibited feedback (inverse) connectivity. Even though synchronous and long-latency correlations were excluded, feed-forward correlation between CA3-CA1 pairs was identified in 1071 (26%) of 4070 total pairs, which favorably compares to reports of 20%–25% feed-forward CA3-CA1 correlation noted in published animal studies.CONCLUSIONSThis study demonstrates the ability to record neurons in vivo from specified regions and subfields of the human brain. As brain-machine interface and neural prosthetic research continues to expand, it is necessary to be able to identify recording and stimulation sites within neural circuits of interest.

Download Full-text

Depth Electrode Guided Anterior Insulectomy: 2-Dimensional Operative Video

Operative Neurosurgery ◽

10.1093/ons/opab112 ◽

2021 ◽

Author(s):

Mauricio Mandel ◽

Layton Lamsam ◽

Pue Farooque ◽

Dennis Spencer ◽

Eyiyemisi Damisah

Keyword(s):

Right Hemisphere ◽

Preoperative Evaluation ◽

Epileptiform Activity ◽

Neurological Deficits ◽

Depth Electrodes ◽

Depth Electrode ◽

Patient Reported ◽

Frontal Operculum ◽

History Of ◽

Electroencephalogram Eeg

Abstract The insula is well established as an epileptogenic area.1 Insular epilepsy surgery demands precise anatomic knowledge2-4 and tailored removal of the epileptic zone with careful neuromonitoring.5 We present an operative video illustrating an intracranial electroencephalogram (EEG) depth electrode guided anterior insulectomy. We report a 17-yr-old right-handed woman with a 4-yr history of medically refractory epilepsy. The patient reported daily nocturnal ictal vocalization preceded by an indescribable feeling. Preoperative evaluation was suggestive of a right frontal-temporal onset, but the noninvasive results were discordant. She underwent a combined intracranial EEG study with a frontal-parietal grid, with strips and depth electrodes covering the entire right hemisphere. Epileptiform activity was observed in contact 6 of the anterior insula electrode. The patient consented to the procedure and to the publication of her images. A right anterior insulectomy was performed. First, a portion of the frontal operculum was resected and neuronavigation was used for the initial insula localization. However, due to unreliable neuronavigation (ie, brain shift), the medial and anterior borders of the insular resection were guided by the depth electrode reference. The patient was discharged 3 d after surgery with no neurological deficits and remains seizure free. We demonstrate that depth electrode guided insular surgery is a safe and precise technique, leading to an optimal outcome.

Download Full-text

Medically resistant pediatric insular-opercular/perisylvian epilepsy. Part 1: invasive monitoring using the parasagittal transinsular apex depth electrode

Journal of Neurosurgery Pediatrics ◽

10.3171/2016.4.peds15636 ◽

2016 ◽

Vol 18 (5) ◽

pp. 511-522 ◽

Cited By ~ 13

Author(s):

Alexander G. Weil ◽

Aria Fallah ◽

Evan C. Lewis ◽

Sanjiv Bhatia

Keyword(s):

Epilepsy Surgery ◽

Electrode Placement ◽

Epileptogenic Zone ◽

Drug Resistant ◽

Depth Electrodes ◽

Depth Electrode ◽

Age At Surgery ◽

Feasible Alternative ◽

The Mean ◽

Drug Resistant Epilepsy

OBJECTIVE Insular lobe epilepsy (ILE) is an under-recognized cause of extratemporal epilepsy and explains some epilepsy surgery failures in children with drug-resistant epilepsy. The diagnosis of ILE usually requires invasive investigation with insular sampling; however, the location of the insula below the opercula and the dense middle cerebral artery vasculature renders its sampling challenging. Several techniques have been described, ranging from open direct placement of orthogonal subpial depth and strip electrodes through a craniotomy to frame-based stereotactic placement of orthogonal or oblique electrodes using stereo-electroencephalography principles. The authors describe an alternative method for sampling the insula, which involves placing insular depth electrodes along the long axis of the insula through the insular apex following dissection of the sylvian fissure in conjunction with subdural electrodes over the lateral hemispheric/opercular region. The authors report the feasibility, advantages, disadvantages, and role of this approach in investigating pediatric insular-opercular refractory epilepsy. METHODS The authors performed a retrospective analysis of all children (< 18 years old) who underwent invasive intracranial studies involving the insula between 2002 and 2015. RESULTS Eleven patients were included in the study (5 boys). The mean age at surgery was 7.6 years (range 0.5–16 years). All patients had drug-resistant epilepsy as defined by the International League Against Epilepsy and underwent comprehensive noninvasive epilepsy surgery workup. Intracranial monitoring was performed in all patients using 1 parasagittal insular electrode (1 patient had 2 electrodes) in addition to subdural grids and strips tailored to the suspected epileptogenic zone. In 10 patients, extraoperative monitoring was used; in 1 patient, intraoperative electrocorticography was used alone without extraoperative monitoring. The mean number of insular contacts was 6.8 (range 4–8), and the mean number of fronto-parieto-temporal hemispheric contacts was 61.7 (range 40–92). There were no complications related to placement of these depth electrodes. All 11 patients underwent subsequent resective surgery involving the insula. CONCLUSIONS Parasagittal transinsular apex depth electrode placement is a feasible alternative to orthogonally placed open or oblique-placed stereotactic methodologies. This method is safe and best suited for suspected unilateral cases with a possible extensive insular-opercular epileptogenic zone.

Download Full-text

Robotic Navigated Laser Craniotomy for Depth Electrode Implantation in Epilepsy Surgery: A Cadaver Lab Study

Journal of Neurological Surgery Part A Central European Neurosurgery ◽

10.1055/s-0040-1720998 ◽

2020 ◽

Author(s):

Karl Roessler ◽

Fabian Winter ◽

Tobias Wilken ◽

Ekaterina Pataraia ◽

Magdalena Mueller-Gerbl ◽

...

Keyword(s):

Laser Beam ◽

Epilepsy Surgery ◽

Entry Point ◽

Occipital Bone ◽

Electrode Placement ◽

Target Point ◽

Twist Drill ◽

Electrode Implantation ◽

Depth Electrodes ◽

Depth Electrode

Abstract Objective Depth electrode implantation for invasive monitoring in epilepsy surgery has become a standard procedure. We describe a new frameless stereotactic intervention using robot-guided laser beam for making precise bone channels for depth electrode placement. Methods A laboratory investigation on a head cadaver specimen was performed using a CT scan planning of depth electrodes in various positions. Precise bone channels were made by a navigated robot-driven laser beam (erbium:yttrium aluminum garnet [Er:YAG], 2.94-μm wavelength,) instead of twist drill holes. Entry point and target point precision was calculated using postimplantation CT scans and comparison to the preoperative trajectory plan. Results Frontal, parietal, and occipital bone channels for bolt implantation were made. The occipital bone channel had an angulation of more than 60 degrees to the surface. Bolts and depth electrodes were implanted solely guided by the trajectory given by the precise bone channels. The mean depth electrode length was 45.5 mm. Entry point deviation was 0.73 mm (±0.66 mm SD) and target point deviation was 2.0 mm (±0.64 mm SD). Bone channel laser time was ∼30 seconds per channel. Altogether, the implantation time was ∼10 to 15 minutes per electrode. Conclusion Navigated robot-assisted laser for making precise bone channels for depth electrode implantation in epilepsy surgery is a promising new, exact and straightforward implantation technique and may have many advantages over twist drill hole implantation.

Download Full-text

A new instrument for improved accuracy of stereotactic depth electrode placement

Journal of Neurosurgery ◽

10.3171/jns.1996.85.2.0357 ◽

1996 ◽

Vol 85 (2) ◽

pp. 357-358 ◽

Cited By ~ 1

Author(s):

Richard D. Ashpole ◽

Gavin C. A. Fabinyi ◽

Milos Vosmansky

Keyword(s):

Simple Device ◽

Electrode Placement ◽

Content Type ◽

Depth Electrodes ◽

Depth Electrode ◽

New Instrument ◽

Improved Accuracy ◽

Fine Print

✓ A disadvantage of stereotactic placement of flexible depth electrodes is the risk of inaccurate positioning as a result of electrode movement when the introducer is withdrawn. A simple device that virtually eliminates this error is described.

Download Full-text

A novel miniature robotic device for frameless implantation of depth electrodes in refractory epilepsy

Journal of Neurosurgery ◽

10.3171/2016.5.jns16388 ◽

2017 ◽

Vol 126 (5) ◽

pp. 1622-1628 ◽

Cited By ~ 25

Author(s):

Christian Dorfer ◽

Georgi Minchev ◽

Thomas Czech ◽

Harald Stefanits ◽

Martha Feucht ◽

...

Keyword(s):

Surgical Navigation ◽

Phantom Study ◽

Entry Point ◽

Electrode Placement ◽

Robotic Device ◽

Robot Assisted ◽

Skull Model ◽

Depth Electrodes ◽

Depth Electrode ◽

Superficial Wound

OBJECTIVEThe authors' group recently published a novel technique for a navigation-guided frameless stereotactic approach for the placement of depth electrodes in epilepsy patients. To improve the accuracy of the trajectory and enhance the procedural workflow, the authors implemented the iSys1 miniature robotic device in the present study into this routine.METHODSAs a first step, a preclinical phantom study was performed using a human skull model, and the accuracy and timing between 5 electrodes implanted with the manual technique and 5 with the aid of the robot were compared. After this phantom study showed an increased accuracy with robot-assisted electrode placement and confirmed the robot's ability to maintain stability despite the rotational forces and the leverage effect from drilling and screwing, patients were enrolled and analyzed for robot-assisted depth electrode placement at the authors' institution from January 2014 to December 2015. All procedures were performed with the S7 Surgical Navigation System with Synergy Cranial software and the iSys1 miniature robotic device.RESULTSNinety-three electrodes were implanted in 16 patients (median age 33 years, range 3–55 years; 9 females, 7 males). The authors saw a significant increase in accuracy compared with their manual technique, with a median deviation from the planned entry and target points of 1.3 mm (range 0.1–3.4 mm) and 1.5 mm (range 0.3–6.7 mm), respectively. For the last 5 patients (31 electrodes) of this series the authors modified their technique in placing a guide for implantation of depth electrodes (GIDE) on the bone and saw a significant further increase in the accuracy at the entry point to 1.18 ± 0.5 mm (mean ± SD) compared with 1.54 ± 0.8 mm for the first 11 patients (p = 0.021). The median length of the trajectories was 45.4 mm (range 19–102.6 mm). The mean duration of depth electrode placement from the start of trajectory alignment to fixation of the electrode was 15.7 minutes (range 8.5–26.6 minutes), which was significantly faster than with the manual technique. In 12 patients, depth electrode placement was combined with subdural electrode placement. The procedure was well tolerated in all patients. The authors did not encounter any case of hemorrhage or neurological deficit related to the electrode placement. In 1 patient with a psoriasis vulgaris, a superficial wound infection was encountered. Adequate physiological recordings were obtained from all electrodes. No additional electrodes had to be implanted because of misplacement.CONCLUSIONSThe iSys1 robotic device is a versatile and easy to use tool for frameless implantation of depth electrodes for the treatment of epilepsy. It increased the accuracy of the authors' manual technique by 60% at the entry point and over 30% at the target. It further enhanced and expedited the authors' procedural workflow.

Download Full-text

Freehand placement of depth electrodes using electromagnetic frameless stereotactic guidance

Journal of Neurosurgery Pediatrics ◽

10.3171/2011.8.peds11143 ◽

2011 ◽

Vol 8 (5) ◽

pp. 464-467 ◽

Cited By ~ 8

Author(s):

Carter D. Wray ◽

Diana L. Kraemer ◽

Tong Yang ◽

Sandra L. Poliachik ◽

Andrew L. Ko ◽

...

Keyword(s):

Electrode Placement ◽

Frameless Stereotaxy ◽

Seizure Onset ◽

Presurgical Evaluation ◽

Electromagnetic System ◽

Depth Electrodes ◽

Depth Electrode ◽

Stereotactic Frame ◽

Stereotactic Guidance ◽

Patients With Epilepsy

The presurgical evaluation of patients with epilepsy often requires an intracranial study in which both subdural grid electrodes and depth electrodes are needed. Performing a craniotomy for grid placement with a stereotactic frame in place can be problematic, especially in young children, leading some surgeons to consider frameless stereotaxy for such surgery. The authors report on the use of a system that uses electromagnetic impulses to track the tip of the depth electrode. Ten pediatric patients with medically refractory focal lobar epilepsy required placement of both subdural grid and intraparenchymal depth electrodes to map seizure onset. Presurgical frameless stereotaxic targeting was performed using a commercially available electromagnetic image-guided system. Freehand depth electrode placement was then performed with intraoperative guidance using an electromagnetic system that provided imaging of the tip of the electrode, something that has not been possible using visually or sonically based systems. Accuracy of placement of depth electrodes within the deep structures of interest was confirmed postoperatively using CT and CT/MR imaging fusion. Depth electrodes were appropriately placed in all patients. Electromagnetic-tracking–based stereotactic targeting improves the accuracy of freehand placement of depth electrodes in patients with medically refractory epilepsy. The ability to track the electrode tip, rather than the electrode tail, is a major feature that enhances accuracy. Additional advantages of electromagnetic frameless guidance are discussed.

Download Full-text

Novel Use of Stimulating Fence-Post Technique for Functional Mapping of Subcortical White Matter During Tumor Resection: A Technical Case Series

Operative Neurosurgery ◽

10.1093/ons/opaa027 ◽

2020 ◽

Vol 19 (3) ◽

pp. 264-270 ◽

Cited By ~ 1

Author(s):

Seunggu Jude Han ◽

Zoe Teton ◽

Kunal Gupta ◽

Aaron Kawamoto ◽

Ahmed M Raslan

Keyword(s):

White Matter ◽

Tumor Resection ◽

Case Series ◽

Electrode Placement ◽

Language Mapping ◽

Depth Electrodes ◽

Depth Electrode ◽

Fence Post ◽

Motor And Language Mapping ◽

Functional Morbidity

Abstract Background Maximal safe resection remains a key principle in infiltrating glioma management. Stimulation mapping is a key adjunct for minimizing functional morbidity while “fence-post” procedures use catheters or dye to mark the tumor border at the start of the procedure prior to brain shift. Objective To report a novel technique using stereotactically placed electrodes to guide tumor resection near critical descending subcortical fibers. Methods Navigated electrodes were placed prior to tumor resection along the deep margin bordering presumed eloquent tracts. Stimulation was administered through these depth electrodes for subcortical motor and language mapping. Results Twelve patients were included in this preliminary technical report. Seven patients (7/12, 58%) were in asleep cases, while the other 5 cases (5/12, 42%) were performed awake. Mapping of motor fibers was performed in 8 cases, and language mapping was done in 1 case. In 3 cases, both motor and language mapping were performed using the same depth electrode spanning corticospinal tract and the arcuate fasciculus. Conclusion Stereotactic depth electrode placement coupled with stimulation mapping of white matter tracts can be used concomitantly to demarcate the border between deep tumor margins and eloquent brain, thus helping to maximize extent of resection while minimizing functional morbidity.

Download Full-text

Robotic image-guided depth electrode implantation in the evaluation of medically intractable epilepsy

Neurosurgical FOCUS ◽

10.3171/foc/2008/25/9/e19 ◽

2008 ◽

Vol 25 (3) ◽

pp. E19 ◽

Cited By ~ 19

Author(s):

William J. Spire ◽

Barbara C. Jobst ◽

Vijay M. Thadani ◽

Peter D. Williamson ◽

Terrance M. Darcey ◽

...

Keyword(s):

Intractable Epilepsy ◽

Robotic System ◽

Electrode Placement ◽

Seizure Onset ◽

Electrode Implantation ◽

Grid Electrode ◽

Image Guided ◽

Depth Electrodes ◽

Depth Electrode ◽

Time Period

Object The authors describe their experience with a technique for robotic implantation of depth electrodes in patients concurrently undergoing craniotomy and placement of subdural monitoring electrodes for the evaluation of intractable epilepsy. Methods Patients included in this study underwent evaluation in the Dartmouth Surgical Epilepsy Program and were recommended for invasive seizure monitoring with depth electrodes between 2006 and the present. In all cases an image-guided robotic system was used during craniotomy for concurrent subdural grid electrode placement. A total of 7 electrodes were placed in 4 patients within the time period. Results Three of 4 patients had successful localization of seizure onset, and 2 underwent subsequent resection. Of the patients who underwent resection, 1 is now seizure free, and the second has only auras. There was 1 complication after subpial grid placement but no complications related to the depth electrodes. Conclusions Robotic image-guided placement of depth electrodes with concurrent craniotomy is feasible, and the technique is safe, accurate, and efficient.

Download Full-text

Accuracy and Workflow Improvements for Responsive Neurostimulation Hippocampal Depth Electrode Placement Using Robotic Stereotaxy

Frontiers in Neurology ◽

10.3389/fneur.2020.590825 ◽

2020 ◽

Vol 11 ◽

Author(s):

Patrick J. Karas ◽

Nisha Giridharan ◽

Jeffrey M. Treiber ◽

Marc A. Prablek ◽

A. Basit Khan ◽

...

Keyword(s):

Prone Position ◽

Seizure Frequency ◽

Supine Position ◽

Human Error ◽

Electrode Placement ◽

Implantation Technique ◽

Radial Error ◽

Depth Electrodes ◽

Depth Electrode ◽

Early Results

Background: Robotic stereotaxy is increasingly common in epilepsy surgery for the implantation of stereo-electroencephalography (sEEG) electrodes for intracranial seizure monitoring. The use of robots is also gaining popularity for permanent stereotactic lead implantation applications such as in deep brain stimulation and responsive neurostimulation (RNS) procedures.Objective: We describe the evolution of our robotic stereotactic implantation technique for placement of occipital-approach hippocampal RNS depth leads.Methods: We performed a retrospective review of 10 consecutive patients who underwent robotic RNS hippocampal depth electrode implantation. Accuracy of depth lead implantation was measured by registering intraoperative post-implantation fluoroscopic CT images and post-operative CT scans with the stereotactic plan to measure implantation accuracy. Seizure data were also collected from the RNS devices and analyzed to obtain initial seizure control outcome estimates.Results: Ten patients underwent occipital-approach hippocampal RNS depth electrode placement for medically refractory epilepsy. A total of 18 depth electrodes were included in the analysis. Six patients (10 electrodes) were implanted in the supine position, with mean target radial error of 1.9 ± 0.9 mm (mean ± SD). Four patients (8 electrodes) were implanted in the prone position, with mean radial error of 0.8 ± 0.3 mm. The radial error was significantly smaller when electrodes were implanted in the prone position compared to the supine position (p = 0.002). Early results (median follow-up time 7.4 months) demonstrate mean seizure frequency reduction of 26% (n = 8), with 37.5% achieving ≥50% reduction in seizure frequency as measured by RNS long episode counts.Conclusion: Prone positioning for robotic implantation of occipital-approach hippocampal RNS depth electrodes led to lower radial target error compared to supine positioning. The robotic platform offers a number of workflow advantages over traditional frame-based approaches, including parallel rather than serial operation in a bilateral case, decreased concern regarding human error in setting frame coordinates, and surgeon comfort.

Download Full-text

Invasive Insular Sampling in Pediatric Epilepsy: A Single-Institution Experience

Operative Neurosurgery ◽

10.1093/ons/opx253 ◽

2017 ◽

Vol 15 (3) ◽

pp. 310-317 ◽

Cited By ~ 2

Author(s):

Luke D Tomycz ◽

Andrew T Hale ◽

Ali S Haider ◽

Dave F Clarke ◽

Mark R Lee

Keyword(s):

Insular Cortex ◽

Clinical Information ◽

Electrode Placement ◽

Pediatric Epilepsy ◽

Seizure Onset ◽

Single Institution ◽

Invasive Treatment ◽

Depth Electrodes ◽

Depth Electrode ◽

Electrode Insertion

Abstract BACKGROUND It has been increasingly recognized that the insular cortex plays an important role in frontotemporal-parietal epilepsy in children. The insula, however, cannot be properly interrogated with conventional subdural grids, and its anatomy makes it difficult to implicate the insula with semiology or noninvasive modalities. Frame-based, stereotactic placement of insular depth electrodes for direct extraoperative monitoring is a relatively low-risk maneuver that allows for conclusive interrogation of this region, and, in select cases, can easily be replaced with a laser applicator for minimally invasive treatment via thermoablation. OBJECTIVE To describe the largest reported series of pediatric patients with refractory epilepsy undergoing insular depth electrode placement. METHODS We used current procedural terminology billing records to identify cases of depth electrode insertion performed at our institution. Clinical information from patients undergoing invasive insular sampling was then retrospectively collected. RESULTS Seventy-four insular depth electrodes were placed in 49 patients for extraoperative, inpatient monitoring. The decision to place insular depth electrodes was determined by a multidisciplinary epilepsy team. In 65.3% of cases, direct invasive sampling implicated the insula in seizure onset and prompted either thermoablation or surgical resection of some portion of the insula. There were no serious adverse effects or complications associated with the placement of insular depth electrodes. CONCLUSION Given the low morbidity of insular depth electrode insertion and the high proportion of patients who exhibited insular involvement, it is worth considering whether insular depth electrodes should be part of the standard presurgical evaluation in children with treatment-refractory frontotemporal-parietal epilepsy.

Download Full-text