Direct visualization of microwires in hybrid depth electrodes using high‐resolution photon‐counting CT

Abstract

Hybrid depth electrodes are increasingly being used for epilepsy monitoring and human neurophysiology research. Microwires extending from the tip of the Behnke‐Fried (BF) electrode into (sub)cortical areas allow to isolate single neurons and perform microstimulation. Conventional CT or MRI visualize the entire microwire bundle as an artifact extending from the BF electrode tip with low resolution, without proper identification of individual microwires. We illustrate the first direct visualization method of individual microwires using high‐resolution photon‐counting CT (PCCT). Coregistration of the PCCT scan with a preoperative MRI can visualize individual wires directly in cortex, which is an advantage as it provides feedback on the accuracy of the implantation method and can guide future implantations. This PCCT technique allows for accurately depicting individual microwires which could be relevant for neuroscientific research through improved visualization and implantation of specific cortical and subcortical brain areas.

Plain Language Summary

Researchers are using hybrid depth electrodes to study epilepsy and brain activity. These electrodes, called Behnke‐Fried (BF) electrodes, have microwires at the tip that can record single neurons and stimulate brain areas. Regular CT or MRI scans do not show the individual microwires clearly. The authors use a new high‐resolution photon‐counting CT (PCCT) technique, which can show each individual microwire in the brain. By combining PCCT with MRI, the authors can precisely see where the microwires are located. This could improve future implantation surgeries and brain research.

1. INTRODUCTION

Intracranial depth electrodes are increasingly being used for epilepsy monitoring and human electrophysiology research. ¹ , ² Hybrid depth electrodes refer to the combination of both macro‐ and microelectrodes in the same electrode shaft. The Behnke‐Fried (BF) electrode is the most commonly used hybrid depth electrode and consists of an outer shaft with macrocontacts through which an inner wire bundle with nine 40‐μm platinum–iridium microwires (microcontacts) is advanced, protruding in multiple directions from the electrode tip. ¹ , ³ The individual microwires are cut at certain lengths before implantation and should be targeted in gray matter before neural spiking activity can be obtained, a delicate procedure of millimeter precision. ⁴ The advantage of adding microelectrodes lies in its superior spatial resolution by recording neuronal spiking activity (multi‐ and/or single‐unit activity), ⁵ which has led to significant advances in cognitive neuroscience and epilepsy research. ¹ , ⁵ , ⁶ Precise localization of the depth electrodes is the first critical step in neurophysiological research and forms the basis for anatomofunctional correlations. ⁷ Macrocontacts can be directly localized on postoperative magnetic resonance imaging (MRI) or computed tomography (CT) showing an extensive metal artifact, the latter being coregistered with the preoperative MRI for localization. ⁷ Localizing macrocontacts based on some extent of artifact does not pose a problem in terms of the precision of correlating anatomical and electrophysiological features, since macrocontacts have a size of a few mm and record from a very large neuronal population in a larger (sub)cortical area. ² For microwires, drawing correlations between neural spiking activity and precise anatomical subregions is of the utmost importance in neuroscientific research and for neuromodulation purposes. ⁸ Currently, visualization of microwires relies on detection of a bundle of artifact extending from the electrode tip on the coregistered MRI‐CT images, without millimeter anatomical precision. ⁸ , ⁹ This is especially relevant for brain structures such as the hippocampus, with its different subfields in close proximity due to anatomical folding and sulci. Currently, these microwires are often assigned to certain anatomical subregions, but without proper visualization of their splayed pattern. For instance, the entire microwire bundle is often identified as one structural entity and is subsequently mapped on only one specific anatomical subregion. Previous research with low resolution imaging already showed that diverging wires can be mapped on distinct anatomofunctional subregions using a computational unfolding technique of the involved brain area. ⁸ However, this method fails to appreciate the played pattern of the entire bundle consisting of nine wires in different directions. Proper visualization of wires could (i) provide direct feedback on the implantation technique and guide future implantations, and (ii) directly show the intracortical localization is specific brain areas.

In contrast to conventional CT scanner detectors, photon‐counting detectors directly convert all x‐ray photons into electrical signals (instead of first converting x‐rays into lower energy visible photons in a scintillator layer, which are then absorbed by a photodiode array). ¹⁰ This technique leads to enhanced contrast‐to‐noise ratio, spatial resolution and artifact reduction. ¹⁰ Specifically for neuroscience, PCCT has been able to directly visualize directional deep brain stimulation lead segments and markers. ¹¹

In this report, we illustrate the first use of high‐resolution PCCT for enhanced visualization of microwires, which can then be coregistered with MRI. This technique can be directly implemented in existing electrode localization pipelines in neuroscience departments.

2. MATERIALS AND METHODS

We employ a photon‐counting CT scanner (Alpha with Quantum Technology®, Siemens Healthineers, Erlangen, Germany) with the following CT brain protocol: Scan mode: RoutineSpiralAdultHeadQuantumPlus; Tube Voltage: 120 kV; Effective mAS: 320; CARE dose off; Pitch: 0.35; Rotation Time: 0.50 s; Acquisition 144 × 0.40 mm; Reconstructions: slice thickness 0.4 mm, slice increment 0.2 mm; Kernel QR40 and HR60. An epilepsy patient was implanted with six depth electrodes (two hybrid BF electrodes and four Spencer Probe depth electrodes, Ad‐Tech® Medical Instrument Corporation, Wisconsin, USA) in multiple target locations. The microwire bundles were implanted in the supplementary motor area and the posterior cingulate cortex. The bone window Iterative Metal Artifact Reduction (iMAR) images and spectral images were used for visualization (Xero® Universal Viewer) and for fusion with the preoperative 3T T1WI MRI using a standard neuronavigation software package (Brainlab Elements© software, Munich, Germany), widely available in neurosurgical departments. Both software packages allow for in‐line image reconstruction to depict the splayed pattern of the microwires. Using the blending mode in the trajectory viewer (Brainlab Elements©), the electrode can be visualized on the T1WI MRI.

3. RESULTS

The microwires of the BF electrode extend from the electrode tip in a splayed pattern in different directions (Figure 1A). Using PCCT, individual wires can be clearly visualized both on iMAR images (Figure 1B; first and second row) and on standard spectral images (Figure 1B; third row). In‐line reconstruction of images along the electrode shaft allows to obtain detailed images of the microwire bundle along its course. This allows to identify single microwires splayed in different directions (Figure 1C,D; from top to bottom corresponding to consecutive sections of the entire wire bundle from the proximal to the distal end). After fusion with MRI, individual wires can be clearly localized in the cortex (Figure 1E,F). Again, using in‐line images, the splayed pattern of the wires can be depicted on MRI. An individual wire can also be accurately localized in an adjacent sulcus, extending outside of the cortex, from which it cannot record neural activity (Figure 1E; second column).

FIGURE 1.

Visualization of microwires with photon‐counting CT (PCCT). (A) Intraoperative image depicting the splayed pattern of the microwire bundle extending from the tip of the Behnke‐Fried (BF) electrode. (B) Rows 1 and 2 show PCCT iMAR images with the individual microwires extending from the tip. Row 3 depicts a PCCT spectral image with high signal‐to‐noise ratio for microwire visualization. (C, D) In‐line views along the trajectory of two BF electrodes (from top to bottom depicting serial images of the microwire bundle from its proximal to its distal end), clearly showing the splayed pattern of individual microwires. (E) Coregistered PCCT images with preoperative 3D T1 MRI in Brainlab Elements® software, clearly depict an individual microwire in the cortex, and one microwire in the sulcus (left wire on the figure). The yellow inset depicts the section at the level of the yellow line. In the left section (more proximal in the bundle), the splayed pattern of the individual wires remains visible on MRI. In the right section (more distal in the bundle), the extracortical (intrasulcal) localization of one wire is visible. (F) Intracortical visualization of microwires in fused CT‐MRI images in a different brain area.

4. DISCUSSION

Here we show that direct visualization of individual microwires of BF electrodes is possible using high‐resolution PCCT, as compared to the current method of visualizing the entire microwire bundle based on an artifact with less resolution using conventional CT or MRI. Using standard coregistration methods, the individual contacts can be very precisely located in gray matter. The main advantage lies within this intracortical visualization, which provides direct feedback on the accuracy of the implantation method, and which could be potentially relevant for neuroscientific research. The current drawback of PCCT is its availability, but the benefits have been shown in multiple areas and will quickly lead to its widespread use. ¹⁰ The main limitation for BF electrodes remains that we currently do not have a means of mapping the individual wires to specific electrode channels, thereby limiting more detailed anatomofunctional correlations.

AUTHOR CONTRIBUTIONS

Conceptualization: Steven Smeijers, Thomas Decramer, and Tom Theys. Data curation: Steven Smeijers, Walter Coudyzer, Elina Keirse, and Vasiliki Bougou. Formal analysis: Steven Smeijers, Walter Coudyzer, Elina Keirse, and Vasiliki Bougou. Funding acquisition: Steven Smeijers and Tom Theys. Investigation: Steven Smeijers and Walter Coudyzer. Methodology: Steven Smeijers, Walter Coudyzer, and Thomas Decramer. Supervision: Thomas Decramer and Tom Theys. Visualization: Steven Smeijers, Walter Coudyzer, Elina Keirse, and Vasiliki Bougou. Writing – original draft: Steven Smeijers, Elina Keirse, and Vasiliki Bougou. Writing – review and editing: Walter Coudyzer, Thomas Decramer, and Tom Theys.

FUNDING INFORMATION

This work was supported by Fonds Wetenschappelijk Onderzoek (FWO). Steven Smeijers received a FWO PhD fellowship fundamental research (project number 11K8923N) and Tom Theys received a FWO fundamental clinical mandate (project number 1830722 N).

CONFLICT OF INTEREST STATEMENT

None of the authors has any conflict of interest to disclose.

COMPLIANCE WITH ETHICS GUIDELINES

Ethical approval was obtained from the institutional Ethical Committee UZ/KU Leuven (reference number s53126; date of positive advice for latest modification of the protocol: August 2nd 2023; date of positive advice for the permission for interim reporting of results: August 22nd 2023) and written informed consent was provided by the participant prior to inclusion (date of enrollment: January 15th 2024). We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.

Smeijers S, Coudyzer W, Keirse E, Bougou V, Decramer T, Theys T. Direct visualization of microwires in hybrid depth electrodes using high‐resolution photon‐counting CT . Epilepsia Open. 2024;9:2518–2521. 10.1002/epi4.13080

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.