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Simultaneous intracranial EEG and functional MRI (icEEG-fMRI) recordings in humans, whereby EEG is recorded from electrodes implanted inside the cranium during fMRI scanning, were made possible following safety studies on test phantoms and our specification of a rigorous data acquisition protocol. In parallel with this work, other investigations in our laboratory revealed the damage caused by the EEG electrode implantation procedure at the cellular level. The purpose of this report is to further explore the safety of performing MRI, including simultaneous icEEG-fMRI data acquisitions, in the presence of implanted intra-cranial EEG electrodes, by presenting some histopathological and heat-shock immunopositive labeling observations in surgical tissue samples from patients who underwent the scanning procedure. We performed histopathology and heat shock protein expression analyses on surgical tissue samples from nine patients who had been implanted with icEEG electrodes. Three patients underwent icEEG-fMRI and structural MRI (sMRI); three underwent sMRI only, all at similar time points after icEEG implantation; and three who did not undergo functional or sMRI with icEEG electrodes. The histopathological findings from the three patients who underwent icEEG-fMRI were similar to those who did not, in that they showed no evidence of additional damage in the vicinity of the electrodes, compared to cases who had no MRI with implanted icEEG electrodes. This finding was similar to our observations in patients who only underwent sMRI with implanted icEEG electrodes. This work provides unique evidence on the safety of functional MRI in the presence of implanted EEG electrodes. In the cases studied, icEEG-fMRI performed in accordance with our protocol based on low-SAR (≤0.1 W/kg) sequences at 1.5T using a head-transmit RF coil, did not result in measurable additional damage to the brain tissue in the vicinity of implanted electrodes. Furthermore, while one cannot generalize the results of this study beyond the specific electrode implantation and scanning conditions described herein, we submit that our approach is a useful framework for the post-hoc safety assessment of MR scanning with brain implants.

We have recently performed simultaneous intracranial EEG and fMRI recordings (icEEG–fMRI) in patients with epilepsy. In this technical note, we examine limited thermometric data for potential electrode heating during our protocol and found that heating was ≤0.1°C in-vitro at least 10 fold less than in-vivo limits. We quantify EEG quality, which can be degraded by MRI scanner-induced artefacts, and fMRI image (gradient echo echo-planar imaging: GE-EPI) signal quality around the electrodes, which can be degraded by electrode interactions with B1 (radiofrequency) and B0 (static) magnetic fields. We recorded EEG outside and within the MRI scanner with and without scanning. EEG quality was largely preserved during scanning and in particular heartbeat-related artefacts were small compared to epileptic events. To assess the GE-EPI signal reduction around the electrodes, we compared image signal intensity along paths into the brain normal to its surface originating from the individual platinum–iridium electrode contacts. GE-EPI images were obtained at 1.5T with an echo time (TE) of 40ms and repetition time (TR) of 3000ms and a slice thickness of 2.5mm. We found that GE-EPI signal intensity reduction was confined to a 10mm radius and that it was reduced on average by less than 50% at 5mm from the electrode contacts. The GE-EPI image signal reduction also varied with electrode orientation relative to the MRI scanner axes; in particular, cortical grid contacts with a normal along the scanner's main magnetic field (B0) axis have higher artefact levels relative to those with a normal perpendicular to the z-axis. This suggests that the artefacts were predominantly susceptibility-related rather than due to B1 interactions. This information can be used to guide interpretation of results of icEEG–fMRI experiments proximal to the electrodes, and to optimise artefact reduction strategies.

Stereoelectroencephalography is a powerful intracerebral EEG recording method for the presurgical evaluation of epilepsy. It consists in implanting depth electrodes in the patient’s brain to record electrical activity and map the epileptogenic zone, which should be resected to render the patient seizure-free. Stereoelectroencephalography has high spatial accuracy and signal-to-noise ratio but remains limited in the coverage of the explored brain regions. Thus, the implantation might provide a suboptimal sampling of epileptogenic regions. We investigate the potential of improving a suboptimal stereoelectroencephalography recording by performing source localization on stereoelectroencephalography signals. We propose combining independent component analysis, connectivity measures to identify components of interest, and distributed source modelling. This approach was tested on two patients with two implantations each, the first failing to characterize the epileptogenic zone and the second giving a better diagnosis. We demonstrate that ictal and interictal source localization performed on the first stereoelectroencephalography recordings matches the findings of the second stereo-EEG exploration. Our findings suggest that independent component analysis followed by source localization on the topographies of interest is a promising method for retrieving the epileptogenic zone in case of suboptimal implantation.

•First systematic study on impact of number of icEEG channels on RF heating.•MR thermometry allows measurements of heating over whole icEEG electrode grids.•RF induced heating of icEEG electrodes decreases with number of channels. Many neurological disorders are analyzed and treated with implantable electrodes. Many patients with such electrodes have to undergo MRI examinations – often unrelated to their implant - at the risk of radio-frequency induced heating. The number of electrode contact sites of these implants keeps increasing due to improvements in manufacturing and computational algorithms. Electrode grids with multiple receive channels couple to the RF fields present in MRI, but, due to their proximity, a combination of leads has a coupling response which is not a superposition of the individual leads’ response. To investigate the problem of RF-induced heating of coupled multi-lead implants, temperature mapping was performed on a set of intra-cranial electroencephalogram (icEEG) electrode grid prototypes with increasing number of contact sites (1-16). Additionally, electric field measurements were used to investigate the radio-frequency heating characteristics of the implants in different media combinations, simulating the device being partially immersed inside the patient. MR measurements show RF-induced heating up to 19.6 K for the single electrode, reducing monotonically with larger number of contact sites to a minimum of 0.9 K for the largest grid. The SAR calculated from temperature measurements agrees well with electric field mapping: The same trend is visible for different insertion lengths, however, the energy dissipated by the whole implant varies with the grid size and insertion length. Thus, in the tested circumstances, a larger electrode number either reduced or had a similar risk of RF induced heating, indicating, that the size of electrode grids is a design parameter, which can be used to change an implants RF response and in turn to reduce the risk of RF induced heating and improve the safety of patient with neuro-implants undergoing MRI examinations.

Simultaneous intracranial EEG and functional MRI (icEEG-fMRI) recordings in humans, whereby EEG is recorded from electrodes implanted inside the cranium during fMRI scanning, were made possible following safety studies on test phantoms and our specification of a rigorous data acquisition protocol. In parallel with this work, other investigations in our laboratory revealed the damage caused by the EEG electrode implantation procedure at the cellular level. The purpose of this report is to further explore the safety of performing MRI, including simultaneous icEEG-fMRI data acquisitions, in the presence of implanted intra-cranial EEG electrodes, by presenting some histopathological and heat-shock immunopositive labeling observations in surgical tissue samples from patients who underwent the scanning procedure. We performed histopathology and heat shock protein expression analyses on surgical tissue samples from nine patients who had been implanted with icEEG electrodes. Three patients underwent icEEG-fMRI and structural MRI (sMRI); three underwent sMRI only, all at similar time points after icEEG implantation; and three who did not undergo functional or sMRI with icEEG electrodes. The histopathological findings from the three patients who underwent icEEG-fMRI were similar to those who did not, in that they showed no evidence of additional damage in the vicinity of the electrodes, compared to cases who had no MRI with implanted icEEG electrodes. This finding was similar to our observations in patients who only underwent sMRI with implanted icEEG electrodes. This work provides unique evidence on the safety of functional MRI in the presence of implanted EEG electrodes. In the cases studied, icEEG-fMRI performed in accordance with our protocol based on low-SAR (≤0.1 W/kg) sequences at 1.5T using a head-transmit RF coil, did not result in measurable additional damage to the brain tissue in the vicinity of implanted electrodes. Furthermore, while one cannot generalize the results of this study beyond the specific electrode implantation and scanning conditions described herein, we submit that our approach is a useful framework for the post-hoc safety assessment of MR scanning with brain implants.

Objective Postimplantation assessment of the position of depth EEG electrodes for intracerebral recordings in patients with refractory focal epilepsy can be performed with MRI or with CT after coregistration to a preimplantation MRI. While both methods offer risks and advantages, postimplantation MRI risks depend on the electrode heating profile under different MRI conditions. We aimed to assess the MRI‐related heating of Dixi microdeep electrodes at 1.5T in multiple electrode configurations and with varying levels of radiofrequency (RF) power. Methods In vitro tests of heating due to RF power deposition were performed according to the F2182‐19e2 standard from the ASTM (American Society for Testing and Materials International). A 10‐contact Dixi microdeep electrode was inserted into the gel within the ASTM head–torso phantom, and the temperature was recorded from selected electrode contacts during MRI. Tests were performed with the electrode positioned in various locations in straight and coiled configurations, with coil diameters from 6 to 25 cm. MRI was conducted on a 1.5T Philips Achieva scanner using the transmit–receive body coil. Results Significant heating was observed for all configurations where more than 12 cm of the electrode was in the RF coil, apart from those with an applied specific absorption rate (SAR) ≤0.16 W/kg and with additional coiling of the electrode lead using a diameter of ≤6 cm. The worst‐case configurations, reaching a maximum temperature of 70°C (temperature rise 48°C), occurred where the electrode end was straight or looped with a large‐diameter (25 cm) loop. Heating was greatest in the contact furthest from the tip. Significance Dixi microdeep electrodes demonstrate heating levels capable of causing serious injury during MRI, but using a conservative SAR limit of 0.1 W/kg and coiling the electrode lead to a diameter of ≤6 cm appears to reduce the heating risk. Plain Language Summary Electrodes positioned within the brain for planning epilepsy surgery can heat up during MRI. Using a standard test object mimicking the electrical properties of the human body, we measured heating of Dixi microdeep depth electrodes in different positions and orientations and with varying levels of radiofrequency power. We found substantial heating apart from when the radiofrequency power was greatly restricted or when the lead was tightly coiled. Different electrode contacts showed drastically different heating, and heating levels capable of causing serious injury were measured during MRI.

The acquisition of electroencephalography (EEG) concurrently with functional magnetic resonance imaging (fMRI) requires a careful consideration of the health hazards resulting from interactions between the scanner’s electromagnetic fields and EEG recording equipment. The primary safety concern is excessive RF-induced heating of the tissue in the vicinity of electrodes. We have previously demonstrated that concurrent intracranial EEG (icEEG) and fMRI data acquisitions (icEEG-fMRI) can be performed with acceptable risk in specific conditions using a head RF transmit coil. Here, we estimate the potential additional heating associated with the addition of scalp EEG electrodes using a body transmit RF coil. In this study, electrodes were placed in clinically realistic positions on a phantom in two configurations: (1) icEEG electrodes only, and (2) following the addition of subdermal scalp electrodes. Heating was measured during MRI scans using a body transmit coil with a high specific absorption rate (SAR), TSE (turbo spin echo), and low SAR gradient-echo EPI (echo-planar imaging) sequences. During the application of the high-SAR sequence, the maximum temperature change for the intracranial electrodes was +2.8 °C. The addition of the subdural scalp EEG electrodes resulted in a maximum temperature change for the intracranial electrodes of 2.1 °C and +0.6 °C across the scalp electrodes. For the low-SAR sequence, the maximum temperature increase across all intracranial and scalp electrodes was +0.7 °C; in this condition, the temperature increases around the intracranial electrodes were below the detection level. Therefore, in the experimental conditions (MRI scanner, electrode, and wire configurations) used at our centre for icEEG-fMRI, adding six scalp EEG electrodes did not result in significant additional localised RF-induced heating compared to the model using icEEG electrodes only.

The application of intracranial electroencephalography (icEEG) recording during functional magnetic resonance imaging (icEEG-fMRI) has allowed the study of the hemodynamic correlates of epileptic activity and of the neurophysiological basis of the blood oxygen level-dependent (BOLD) signal. However, the applicability of this technique is affected by data quality issues such as signal drop out in the vicinity of the implanted electrodes. In our center we have limited the technique to a quadrature head transmit and receive RF coil following the results of a safety evaluation. The purpose of this study is to gather further safety-related evidence for performing icEEG-fMRI using a body RF-transmit coil, to allow the greater flexibility afforded by the use of modern, high-density receive arrays, and therefore parallel imaging with benefits such as reduced signal drop-out and distortion artifact. Specifically, we performed a set of empirical temperature measurements on a 1.5T Siemens Avanto MRI scanner with the body RF-transmit coil in a range of electrode and connector cable configurations. The observed RF-induced heating during a high-SAR sequence was maximum in the immediate vicinity of a depth electrode located along the scanner's central axis (range: 0.2-2.4°C) and below 0.5°C at the other electrodes. Also for the high-SAR sequence, we observed excessive RF-related heating in connection cable configurations that deviate from our recommended setup. For the low-SAR sequence, the maximum observed temperature increase across all configurations was 0.3°C. This provides good evidence to allow simultaneous icEEG-fMRI to be performed utilizing the body transmit coil on the 1.5T Siemens Avanto MRI scanner at our center with acceptable additional risk by following a well-defined protocol.

Scalp EEG recordings and the classification of interictal epileptiform discharges (IED) in patients with epilepsy provide valuable information about the epileptogenic network, particularly by defining the boundaries of the “irritative zone” (IZ), and hence are helpful during pre-surgical evaluation of patients with severe refractory epilepsies. The current detection and classification of epileptiform signals essentially rely on expert observers. This is a very time-consuming procedure, which also leads to inter-observer variability. Here, we propose a novel approach to automatically classify epileptic activity and show how this method provides critical and reliable information related to the IZ localization beyond the one provided by previous approaches. We applied Wave_clus, an automatic spike sorting algorithm, for the classification of IED visually identified from pre-surgical simultaneous Electroencephalogram–functional Magnetic Resonance Imagining (EEG–fMRI) recordings in 8 patients affected by refractory partial epilepsy candidate for surgery. For each patient, two fMRI analyses were performed: one based on the visual classification and one based on the algorithmic sorting. This novel approach successfully identified a total of 29 IED classes (compared to 26 for visual identification). The general concordance between methods was good, providing a full match of EEG patterns in 2 cases, additional EEG information in 2 other cases and, in general, covering EEG patterns of the same areas as expert classification in 7 of the 8 cases. Most notably, evaluation of the method with EEG–fMRI data analysis showed hemodynamic maps related to the majority of IED classes representing improved performance than the visual IED classification-based analysis (72% versus 50%). Furthermore, the IED-related BOLD changes revealed by using the algorithm were localized within the presumed IZ for a larger number of IED classes (9) in a greater number of patients than the expert classification (7 and 5, respectively). In contrast, in only one case presented the new algorithm resulted in fewer classes and activation areas. We propose that the use of automated spike sorting algorithms to classify IED provides an efficient tool for mapping IED-related fMRI changes and increases the EEG–fMRI clinical value for the pre-surgical assessment of patients with severe epilepsy. •We used a new approach for classifying epileptic spikes in 8 patients.•We compared the results with visual classification using EEG–fMRI maps.•The performance for EEG–fMRI analysis improved from 46 to 72%.•IED-cluster localization matched presumed IZ in additional 4 classes and 1 patient.

Introduction Phase II monitoring with intracranial electroencephalography (ICEEG) occasionally requires bilateral placement of subdural (SD) strips, grids, and/or depth electrodes. While phase I monitoring often demonstrates a preponderance of unilateral findings, individual studies (video EEG, single photon emission computed tomography [SPECT], and positron emission tomography [PET]) can suggest or fail to exclude a contralateral epileptogenic onset zone. This study describes previously unreported techniques of trans-falcine and sub-frontal insertion of contralateral SD grids and depth electrodes for phase II monitoring in pediatric epilepsy surgery patients when concern about bilateral abnormalities has been elicited during phase I monitoring. Methods Pediatric patients with medically refractory epilepsy undergoing stage I surgery for phase II monitoring involving sub-frontal and/or trans-falcine insertion of SD grids and/or depth electrodes at the senior author’s institution were retrospectively reviewed. Intra-operative technical details of sub-frontal and trans-falcine approaches were studied, while intra-operative complications or events were noted. Operative techniques included gentle subfrontal retraction and elevation of the olfactory tracts (while preserving the relationship between the olfactory bulb and cribriform plate) to insert SD grids across the midline for coverage of the contralateral orbito-frontal regions. Trans-falcine approaches involved accessing the inter-hemispheric space, bipolar cauterization of the anterior falx cerebri below the superior sagittal sinus, and sharp dissection using a blunt elevator and small blade scalpel. The falcine window allowed contralateral SD strip, grid, and depth electrodes to be inserted for coverage of the contralateral frontal regions. Results The study cohort included seven patients undergoing sub-frontal and/or trans-falcine insertion of contralateral SD strip, grid, and/or depth electrodes from February 2012 through June 2015. Five patients (71%) experienced no intra-operative events related to contralateral ICEEG electrode insertion. Intra-operative events of frontal territory venous engorgement (1/7, 14%) due to sacrifice of anterior bridging veins draining into the SSS and avulsion of a contralateral bridging vein (1/7, 14%), probably due to prior anterior corpus callosotomy, each occurred in one patient. There were no intra-operative or peri-operative complications in any of the patients studied. Two patients required additional surgery for supplemental SD strip and/or depth electrodes via burr hole craniectomy to enhance phase II monitoring. All patients proceeded to stage II surgery for resection of ipsilateral epileptogenic onset zones without adverse events. Conclusions Trans-falcine and sub-frontal insertion of contralateral SD strip, grid, and depth electrodes are previously unreported techniques for achieving bilateral frontal coverage in phase II monitoring in pediatric epilepsy surgery. This technique obviates the need for contralateral craniotomy and parenchymal exposure with limited, remediable risks. Larger case series using the method described herein are now necessary.