Visualization of Brain Shift Corrected Functional Magnetic Resonance Imaging Data for Intraoperative Brain Mapping

Abstract

Background: Brain tumor surgery requires careful balance between maximizing tumor excision and preserving eloquent cortex. In some cases, the surgeon may opt to perform an awake craniotomy including intraoperative mapping of brain function by direct cortical stimulation (DCS) to assist in surgical decision-making. Preoperatively, functional magnetic resonance imaging (fMRI) facilitates planning by identification of eloquent brain areas, helping to guide DCS and other aspects of the surgical plan. However, brain deformation (shift) limits the usefulness of preoperative fMRI during surgery. To address this, an integrated visualization method for fMRI and DCS results is developed that is intuitive for the surgeon.

Methods: An image registration pipeline was constructed to display preoperative fMRI data corrected for brain shift overlaid on images of the exposed cortical surface at the beginning and completion of DCS mapping. Preoperative fMRI and DCS data were registered for a range of misalignments, and the residual registration errors were calculated. The pipeline was validated on imaging data from five brain tumor patients who underwent awake craniotomy.

Results: Registration errors were well under 5 mm (the approximate spatial resolution of DCS) for misalignments of up to 25 mm and approximately 10-15°. For rotational misalignments up to 20°, the success rate was 95% for an error tolerance of 5 mm. Failures were negligible for rotational misalignments up to 10°. Good quality registrations were observed for all five patients.

Conclusions: A proof-of-concept image registration pipeline is presented with acceptable accuracy for intraoperative use, providing multimodality visualization with potential benefits for intraoperative brain mapping.

Keywords: 2D, 2-dimensional; 3D, 3-Dimensional; Awake craniotomy; Brain mapping; Brain tumor resection; CT, Computed tomography; DCS, Direct cortical stimulation; Electric stimulation; FOV, Field of view; Functional mapping; MRI, Magnetic resonance imaging; Multimodal imaging; RE, Registration error; Surgical planning; TE, Echo time; TR, Repetition time; fMRI, Functional magnetic resonance imaging.

Figure 1

Proposed image registration pipeline using mutual information as the similarity metric for the correction of brain shift.

Figure 2

Schematic illustrating the in silico experimental testing procedure for 1 iteration. The landmark point (x1,y1) represents ground truth, whereas point (x2,y2) represents the misalignment produced by translation r and random rotation by angle α. The ability of the image registration algorithm to correct for the misalignment was subsequently quantified. See text for details.

Figure 3

Distribution of registration error (RE values) for 5 patients (P1-P5) displayed using box-and-whisker plots for each initial misalignment. Each box-and-whisker plot consists of the interquartile range (IQR, box), median (line inside the box), whiskers extending to 1.5*IQR on both ends and minimum and maximum outliers as shown by symbols in the legend.

Figure 4

Checkerboard images of the 2-dimensional projection (gray) of preoperative hand motor fMRI (blue) and intraoperative cortical surface data (red) for patient P2, shown before and after registration for preDCS (pipeline Module 1). The misregistration and its correction following registration can be easily observed in the zoomed-in grayscale view.

Figure 5

Outputs of the proposed registration pipeline shown for all patients, with additional labeling of DCS sites and delineation of tumor/resection cavity with white dashed line. Each row of images is from the patient indicated on the top left. The first column (preDCS) shows output of pipeline Module 1. For patients P1-P4, fMRI activations of hand motor, and for patient P5 functional magnetic resonance imaging (fMRI) activations of tongue movement (right) and semantic decision tasks (left) are shown on the intraoperative cortical image. The second column (postDCS) shows output of pipeline Module 2, showing fMRI activations overlaid on intraoperative cortical surface with DCS mapping results. The DCS site labels “S,” “H,” “F,” “Ft,” “SA,” “RD,” and “RA” correspond to sites of sensory activation, hand motor, facial twitching, foot motor, speech arrest, reading difficulty, and receptive aphasia, respectively (*marked based on anatomic location).