Comparison of functional MR imaging guidance to electrical cortical mapping for targeting selective motor cortex areas in neuropathic pain: a study based on intraoperative stereotactic navigation

Abstract

Purpose: To assess the concordance between data from functional MR imaging (fMRI) guidance and the intraoperative electrical cortical mapping (iCM) in targeting selective motor cortex areas in refractory neuropathic pain.

Methods: Twenty-one patients (11 women and 10 men; mean age, 55.6 years) with refractory central (ischemic, 8 cases) and neuropathic pain (trigeminal neuropathy, 6 cases; syrinx/amputation/plexus trauma, 7 cases) underwent surgery for the implantation of an epidural electrode for chronic motor cortex stimulation (MCS) with general anesthesia and a frameless neuronavigation system used for the image-guided targeting procedure. All patients were studied by preoperative fMRI and epidural iCM with somatosensory evoked potentials and motor cortex stimulodetection. fMRI investigated systematically motor tasks of both hands and that related to the somatic area (foot or tongue) affected by pain. fMRI data were analyzed with the Statistical Parametric Mapping99 software (initial analysis threshold [AT] corresponding to P < .001), registered in the neuronavigation system and correlated intraoperatively with iCM. Matching of fMRI and iCM was specifically examined, focusing the study on hand mapping.

Results: Concordance between contours of fMRI activation area and iCM in precentral gyrus (mean distance, 3.8 mm) was found in 20/21 patients (95%). Because precision of iCM was suboptimal in 7 patients, concordance for more restrictive values of the AT (P < .0001) was found in only 13 of these 20 patients. Concordance was not found in one patient, as result of image distortion and residual motion artifact.

Conclusions: In this study, fMRI guidance provides information that matches those of an independent functional method. These data illustrate the functional accuracy of fMRI guidance for the operative targeting of selective motor cortex areas in neuropathic pain.

Fig 1.

A, Virtual 3D reconstruction (cortex surfacing method) of the right hemisphere in the navigation workstation showing the integration of data from iCM and fMRI in the case of patient 8. The iCM-defined central sulcus (yellow line), the iCM-defined sensorimotor target of the hand (red diabolo), and the fMRI-activated area after motor tasks of the hand (at initial analysis threshold, green area; at more restrictive values, white cross), the fMRI-activated area after motor of the tongue (at initial analysis threshold, orange area; at more restrictive values, yellow area) projected in the portion of the precentral gyrus anatomically devoted to the face (pink area). The iCM-defined motor target of the hand (red cross) corresponds spatially with the fMRI precentral activation (green area). B, Virtual 3D reconstruction (cortex surfacing method) of the right hemisphere in the navigation workstation showing the integration of data from iCM and fMRI in the case of patient 21. The iCM-defined central sulcus (green line), the iCM-defined sensorimotor target of the hand (red diabolo), the fMRI-activated area after motor tasks of the hand (at initial analysis threshold, violet area; at more restrictive values, white cross), and the fMRI-activated area after motor of the foot (at initial analysis threshold, azure area; at more restrictive values, white cross) projected in the portion of the parasagittal precentral convexity. The iCM-defined motor target of the hand (red cross) corresponds spatially with the fMRI precentral activation (violet area). The significant postcentral activations obtained after sensory activation paradigms of the hand (orange area) and foot (blue area) enable validation of the precentral motor activations of the same segments.

Fig 2.

Axial functional MR imaging sequences showing the bilateral precentral cortical activation after motor tasks of the left hand in patients 14 (A) and 20 (B), amputated from the right upper limb (blue cross, enabling correlation between both images on B). This activation is obtained for analysis threshold corresponding to P values much greater than .0001. Minor differences are observed in surface and distribution of the activation between both sides.

Fig 3.

Correlation, in the navigation system, between the iCM-defined targets (center of a 1-cm area between 2 poles of the grid but represented by a red cross) and the contours of the fMRI-defined activation areas (green and pink surfaces for hand and face, respectively, including focus of highest significance [centroid of the blob, black cross] designated as “fMRI target”) at the initial (or more restrictive) analysis threshold corresponding to P < .001 (or P < .0001). These pictures and the surface of cortical activation are only illustrative and do not represent actual data. A, When targets are unambiguous (focal/reproducible/significant/with no artifact), we estimate that they correspond spatially only if the contours of the fMRI-activated area include the target of highest iCM wave. B, When repeated iCM recordings provide ambiguous (diffused, not reproducible, altered by artifacts) results (red pointed square crosses), we designate as the iCM target the one defined by the recording presenting the highest amplitude (red cross). If this target is projected within the contours of the fMRI-activated area, we estimate that targets from both techniques corresponded spatially. When no iCM target is available, no comparison is possible. C, When spatial concordance between both targets was obtained with lower thresholds than that corresponding to P < .001 (ie, when P < .01), we estimate that the concordance is not significant.