Elsevier

NeuroImage

Volume 59, Issue 4, 15 February 2012, Pages 3563-3570
NeuroImage

Individualized localization and cortical surface-based registration of intracranial electrodes

https://doi.org/10.1016/j.neuroimage.2011.11.046Get rights and content

Abstract

In addition to its widespread clinical use, the intracranial electroencephalogram (iEEG) is increasingly being employed as a tool to map the neural correlates of normal cognitive function as well as for developing neuroprosthetics. Despite recent advances, and unlike other established brain-mapping modalities (e.g. functional MRI, magneto- and electroencephalography), registering the iEEG with respect to neuroanatomy in individuals—and coregistering functional results across subjects—remains a significant challenge. Here we describe a method which coregisters high-resolution preoperative MRI with postoperative computerized tomography (CT) for the purpose of individualized functional mapping of both normal and pathological (e.g., interictal discharges and seizures) brain activity. Our method accurately (within 3 mm, on average) localizes electrodes with respect to an individual's neuroanatomy. Furthermore, we outline a principled procedure for either volumetric or surface-based group analyses. We demonstrate our method in five patients with medically-intractable epilepsy undergoing invasive monitoring of the seizure focus prior to its surgical removal. The straight-forward application of this procedure to all types of intracranial electrodes, robustness to deformations in both skull and brain, and the ability to compare electrode locations across groups of patients makes this procedure an important tool for basic scientists as well as clinicians.

Highlights

► We describe a method for localizing intracranial electrodes in individuals. ► Post-implant CT was coregistered with pre-implant MRI. ► An optimization algorithm accounted for the brain shift caused by implantation. ► Surface-based methods were used to coregister electrode arrays across patients.

Introduction

In a large subset of patients with complex partial epilepsy, pharmacological intervention is ineffective (Engel et al., 2005). If non-invasive measures (e.g. EEG, PET, fMRI) fail to sufficiently localize the epileptogenic zone or if that zone abuts or overlaps eloquent cortex, arrays of electrodes placed either directly on the cortical surface or into deep structures (e.g. hippocampus, amygdala) may be indicated. Since its inception (Penfield and Jasper, 1954, Engel et al., 2005), iEEG has been the gold-standard method for localizing seizure foci and delineating eloquent cortex in patients with medically-intractable epilepsy. Owing to its high spatiotemporal resolution and simultaneous coverage of wide areas of cortex, iEEG is increasingly being used as a tool to study the neural correlates of normal cognitive function (e.g., Crone et al., 2001, Yoshor et al., 2007, Brugge et al., 2008, Jerbi et al., 2009, Sahin et al., 2009) and examine spontaneous brain activity (e.g., Canolty et al., 2006, He et al., 2008, Cash et al., 2009). It has proven particularly informative in studying certain aspects of brain activity (e.g. gamma-band activity) which are less observable with non-invasive methods (i.e., EEG or MEG). More recently, intracranial electrodes are also being used as a recording platform from which to design brain–computer interfaces for various neuroprosthetic purposes, including communication aids for patients who suffer from amyotrophic lateral sclerosis or stroke (e.g., Wilson et al., 2006, Leuthardt et al., 2006, Felton et al., 2007, Schalk et al., 2008, Schalk, 2010, Shenoy et al., 2008).

For clinical as well as scientific purposes—including seizure-onset localization, eloquent-cortex mapping, and cross-subject comparison, as well as relating results to other neuroanatomical structures (e.g. white matter tracts) and the larger neuroimaging literature—knowledge of electrode location with respect to the patient's individual neuroanatomy is critical. This is especially true given the spatial specificity of iEEG (due to its proximity to neural generators). Despite its importance, registering iEEG with a patient's individual cortical folding pattern remains a major challenge. Several solutions to this problem have been proposed, utilizing photography (Wellmer et al., 2002, Mahvash et al., 2007, Dalal et al., 2008), 2D radiography (Miller et al., 2007), postoperative MRI (Bootsveld et al., 1994, Kovalev et al., 2005; Hugh Wang et al., Comprehensive Epilepsy Center, New York University School of Medicine, personal communication), or postoperative CT (Grzeszczuk et al., 1992, Winkler et al., 2000, Noordmans et al., 2001, Nelles et al., 2004, Hunter et al., 2005, Tao et al., 2009, Hermes et al., 2010), each with inherent limitations.

Here, we describe an electrode-localization procedure which combines the coregistration of high-resolution preoperative MRI with postoperative CT and the 3D rendering of each patient's cortical surface (Dale et al., 1999, Fischl et al., 1999a) or volumetric reslicing to align the slice with the long axis of depth-electrode arrays. The parenchymal shift introduced by the implantation of subdural electrodes (Hill et al., 1998, Hill et al., 2000, Hastreiter et al., 2004, Miyagi et al., 2007, Dalal et al., 2008, Hermes et al., 2010), which can often be larger than a centimeter (Hill et al., 1998), potentially causing localization errors at least this large (Dalal et al., 2008), is accounted for by using an optimization algorithm that minimizes an energy function defined by inter-electrode distances and global deformation of electrode configuration. This method minimizes assumptions about the nature of the parenchymal shift introduced by the implant and allows for accurate localization of electrodes near highly convex cortical regions. We extend previous work by providing a procedure for cortical surface-based intersubject registration of each individual's electrode ensemble, allowing for surface-based group analyses of studies utilizing subdural electrodes. Given the fact that subdural electrodes are positioned on the cortical surface, this method of group analysis should prove more accurate when compared to the standard volumetric-based analyses (Collins et al., 1994, Miller et al., 2007, Ritzl et al., 2007, Talairach and Tournoux, 1988). We validate our registration method by comparison with intraoperative photographs, using prominent anatomical landmarks in order to determine the distance between estimated and actual electrode locations in reference to the 3D cortical reconstruction.

Section snippets

Patients

Five patients with medically-intractable epilepsy underwent clinically-indicated invasive monitoring of the seizure focus prior to its surgical removal (Table 1). Patients gave their informed consent, and all procedures were approved by the Institutional Review Boards at Partners Healthcare (Massachusetts General Hospital and Brigham and Women's Hospital) and the Massachusetts Institute of Technology. Prior to electrode implantation, each patient underwent high-resolution T1-weighted MRI. No

Individual localization

Fig. 3B shows the results of our projection method for an individual subject implanted with four 2 × 8 and one 1 × 8 strip arrays. As can be seen in the upper and lower left-hand panels of Fig. 3B, several electrodes are either invisible or outside the brain as defined by the smoothed pial surface. After the snapping procedure outlined in section 2.5 was performed (Fig. 4), the electrodes now appear on the smoothed pial surface (upper right-hand panel of Fig. 3B), and were finally snapped to the

Discussion

The localization of intracranial electrodes is a critical issue in electrocorticography for clinical as well as scientific purposes. We have demonstrated a method for accurately aligning a postoperative CT scan with preoperative MRI for the purpose of individualized localization of semi-chronic intracranial electrodes. The method coregisters preoperative MRI with postoperative CT using a combination of an automatic mutual information-based procedure (Wells et al., 1996) and visual inspection.

Acknowledgments

The authors thank the patients and their families for their participation, Naoro Tanaka and Steve Stufflebeam for providing cortical reconstructions for patients 4 and 5, the neurology staff at both Massachusetts General Hospital and Brigham and Women's Hospital for assistance in data collection as well as Eric Halgren and Thomas Thesen for helpful comments.

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