Elsevier

NeuroImage

Volume 125, 15 January 2016, Pages 515-521
NeuroImage

Three-dimensional localization of cortical electrodes in deep brain stimulation surgery from intraoperative fluoroscopy

https://doi.org/10.1016/j.neuroimage.2015.10.076Get rights and content

Highlights

  • A semi-automated method for estimating ECoG electrode locations in DBS surgery is presented.

  • This method does not require intraoperative CT.

  • An associated software package has been made freely available online.

Abstract

Electrophysiological recordings from subdural electrocorticography (ECoG) electrodes implanted temporarily during deep brain stimulation (DBS) surgeries offer a unique opportunity to record cortical activity for research purposes. The optimal utilization of this important research method relies on accurate and robust localization of ECoG electrodes, and intraoperative fluoroscopy is often the only imaging modality available to visualize electrode locations. However, the localization of a three-dimensional electrode position using a two-dimensional fluoroscopic image is problematic due to the lost dimension orthogonal to the fluoroscopic image, a parallax distortion implicit to fluoroscopy, and variability of visible skull contour among fluoroscopic images. Here, we present a method to project electrodes visible on the fluoroscopic image onto a reconstructed cortical surface by leveraging numerous common landmarks to translate, rotate, and scale coregistered computed tomography (CT) and magnetic resonance imaging (MRI) reconstructed surfaces in order to recreate the coordinate framework in which the fluoroscopic image was acquired, while accounting for parallax distortion. Validation of this approach demonstrated high precision with an average total Euclidian distance between three independent reviewers of 1.65 ± 0.68 mm across 8 patients and 82 electrodes. Spatial accuracy was confirmed by correspondence between recorded neural activity over sensorimotor cortex during hand movement. This semi-automated interface reliably estimates the location of temporarily implanted subdural ECoG electrodes visible on intraoperative fluoroscopy to a cortical surface.

Introduction

Subdural electrocorticography (ECoG) electrodes are useful clinical tools for functional mapping and seizure monitoring that can also provide detailed temporal and spatial information valuable for cognitive neuroscience research. Recent studies have employed the temporary implantation of subdural ECoG electrodes during deep brain stimulation (DBS) electrode implantation surgeries in order to simultaneously record cortical ECoG and subcortical single unit and local field potential (LFP) activity in the intraoperative setting. Initial findings using this technique suggest that patients with movement disorders, including Parkinson's disease (PD) (De Hemptinne et al., 2013, De Hemptinne et al., 2015, Crowell et al., 2012, Whitmer et al., 2012) and essential tremor (ET) (Air et al., 2012), have abnormal oscillatory activity recorded within the structures in the sensorimotor network. However, the lack of a reliable method for localizing the ECoG electrodes on the cortical surface in the absence of intraoperative computed tomography (CT) scanning is a limitation for the expansion of this important research opportunity. The accurate localization of these electrodes is essential for relating the recorded ECoG signals to the anatomical structures responsible for generating them.

Effective methods for the localization of subdural ECoG electrodes have been developed for clinical and research use in patients with medically refractory epilepsy. One common method uses post-operative CT to visualize implanted electrode locations that are then coregistered to their corresponding locations in pre-operative magnetic resonance imaging (MRI) space (Azarion et al., 2014, Hermes et al., 2010, Tao et al., 2009, Ken et al., 2007, Wang et al., 2013). Three-dimensional stereotactic coordinates for each electrode can then be determined on an individual reconstructed MRI. Other methods verify the electrode locations visually on the exposed brain surface with either surgical photographs or a neuro-navigational system and additionally leverages known electrode spacing to calculate the locations of non-exposed electrodes (Dalal et al., 2008, Yang et al., 2012). However, since the subdural ECoG electrodes used during DBS surgeries are only implanted temporarily and are not visible within the cranial opening, intraoperative imaging represents the only opportunity to visualize the implanted subdural electrodes. Upper extremity somatosensory evoked potential phase reversal mapping can also be used to functionally localize ECoG electrodes to the upper extremity representation of the somatosensory cortex in the post-central gyrus, but cannot localize electrodes to non-somatosensory areas of cortex. Of the options for intraoperative imaging, fluoroscopy is most often used during DBS surgeries to verify the final DBS lead position in relation to the stereotactic arc center, since intraoperative CT is not readily available in many DBS programs.

Determining the three-dimensional locations of subdural electrodes from a two-dimensional fluoroscopy image, however, is problematic due to a lack of depth information in the dimension orthogonal to the image orientation. It is possible to regain this dimension by overlaying and aligning the 2-D fluoroscopic image and corresponding 3-D anatomy to recreate the coordinate framework under which the fluoroscopic image was acquired. Many previous cortical electrode localization methods performed this coregistration by assuming that the fluoroscopic image was acquired at a perfectly lateral view (Rowland et al., 2014, Miller et al., 2007b). This assumption may imprecisely fixe rotation along all coordinate axes, limiting the ability to accurately localize cortical electrodes to a particular gyrus. One method that does account for rotation in two of the three coordinate axes utilizes post-operative fluoroscopic images in multiple orientations (Miller et al., 2010), although typically this is cumbersome in the intraoperative setting. These methods also either rely on manual placement of the reconstructed MRI within the inner skull contour (Rowland et al., 2014) or approximate alignment using the anterior–posterior commissure (AC-PC) and inioglabellar line (Miller et al., 2007b, Miller et al., 2010), which can introduce error to the resulting electrode locations. All previous methods additionally do not account for the distortion introduced by the parallax effect implicit in fluoroscopic images, which unrealistically magnifies objects closer to the X-ray source.

We developed a semi-automated method to localize subdural electrodes on a three-dimensional reconstructed brain using intraoperative fluoroscopy obtained during DBS electrode implantation. This method aligns coregistered pre-operative CT and post-operative MRI surfaces with an intraoperative fluoroscopic image in a manner that recreates the coordinate framework of the fluoroscopic image and simulates the parallax distortion to provide accurate and reliable electrode location estimations on the cortical surface. The reproducibility of this method was validated using multiple independent reviewers, and the accuracy of these estimations were confirmed using observed functional cortical activity.

Section snippets

Patients

Eight patients undergoing DBS electrode implantation for the treatment of movement disorders were included in this study (7 male, 1 female, 64.4 ± 1.9 years, mean ± SE). Patient diagnoses included PD (n = 5) and ET (n = 3). DBS electrode targets were either the subthalamic nucleus (STN; n = 4) or the internal globus pallidus (GPi; n = 1) for patients with PD, and the ventral intermediate (Vim) nucleus of the thalamus (n = 3) for patients with ET. Six patients underwent bilateral implantation, and two patients

Results

This technique localized cortical ECoG electrodes temporarily implanted during DBS surgery using routine clinical imaging. We assessed the degree to which independent reviewers could localize cortical electrode contacts to a specific location. In total, each reviewer localized 82 electrode contacts from 9 electrode strips across 8 patients. Average distance from reviewer mean location for all electrodes was 1.25 ± 0.73 mm (mean ± SD) in the medial–lateral direction (x-axis), 0.68 ± 0.39 mm in the

Discussion

Recording cortical activity with subdural electrodes during DBS surgery offers a unique opportunity to gain valuable insight into the electrophysiology of movement disorders and other conditions treated with DBS. Initial electrocorticography (ECoG) studies involving patients with Parkinson's disease and essential tremor have demonstrated the utility of this technique with findings that may improve DBS therapy by supporting the development of adaptive, closed-loop DBS devices (de Hemptinne et

Limitations

Potential users of this method should note that greater variability in electrode location estimations are likely to occur when only one electrode has been implanted, when the lateral fluoroscopic image is less orthogonal to the anterior–posterior course of the strip electrode, and when less of the inner and outer tables of the skull are visible on fluoroscopy. It may be possible to develop a completely automated method with an algorithm that can optimize the alignment of the CT and MRI surface

Conclusion

In order to facilitate further investigation of normal and abnormal cortical activity in patients undergoing DBS surgery, we have produced a semi-automatic interface that enables users to localize subdural electrodes implanted temporarily during surgery onto a 3-D cortical surface using intraoperative fluoroscopy and routine clinical imaging. This platform enables expanded studies of the neurophysiology of disorders treated by DBS.

The following are the supplementary data related to this article.

Acknowledgements

We would like to thank Jim Sweat for his expert assistance in the operating room.

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    1

    These authors contributed equally to this study.

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