Intraoperative subcortical mapping of a language-associated deep frontal tract connecting the superior frontal gyrus to Broca's area in the dominant hemisphere of patients with glioma

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OBJECT

The deep frontal pathway connecting the superior frontal gyrus to Broca's area, recently named the frontal aslant tract (FAT), is assumed to be associated with language functions, especially speech initiation and spontaneity. Injury to the deep frontal lobe is known to cause aphasia that mimics the aphasia caused by damage to the supplementary motor area. Although fiber dissection and tractography have revealed the existence of the tract, little is known about its function. The aim of this study was to determine the function of the FAT via electrical stimulation in patients with glioma who underwent awake surgery.

METHODS

The authors analyzed the data from subcortical mapping with electrical stimulation in 5 consecutive cases (3 males and 2 females, age range 40–54 years) with gliomas in the left frontal lobe. Diffusion tensor imaging (DTI) and tractography of the FAT were performed in all cases. A navigation system and intraoperative MRI were used in all cases. During the awake phase of the surgery, cortical mapping was performed to find the precentral gyrus and Broca's area, followed by tumor resection. After the cortical layer was removed, subcortical mapping was performed to assess language-associated fibers in the white matter.

RESULTS

In all 5 cases, positive responses were obtained at the stimulation sites in the subcortical area adjacent to the FAT, which was visualized by the navigation system. Speech arrest was observed in 4 cases, and remarkably slow speech and conversation was observed in 1 case. The location of these sites was also determined on intraoperative MR images and estimated on preoperative MR images with DTI tractography, confirming the spatial relationships among the stimulation sites and white matter tracts. Tumor removal was successfully performed without damage to this tract, and language function did not deteriorate in any of the cases postoperatively.

CONCLUSIONS

The authors identified the left FAT and confirmed that it was associated with language functions. This tract should be recognized by clinicians to preserve language function during brain tumor surgery, especially for tumors located in the deep frontal lobe on the language-dominant side.

ABBREVIATIONSDTI = diffusion tensor imaging; ECoG = electrocorticography; FAT = frontal aslant tract; IFG = inferior frontal gyrus; IFOF = inferior frontooccipital fascicle; SFG = superior frontal gyrus; SLF = superior longitudinal fascicle; SMA = supplementary motor area.

Article Information

Correspondence Masazumi Fujii, 65 Tsurumai-cho, Showa-ku, Nagoya 466-8550, Japan. email: fujiim@med.nagoya-u.ac.jp.

INCLUDE WHEN CITING Published online March 27, 2015; DOI: 10.3171/2014.10.JNS14945.

DISCLOSURE This study was supported by Grant-in-Aid for Scientific Research (C) 24592158 (KAKENHI). The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

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Figures

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    Case 2. Representative case of the stimulation point adjustment from the intraoperative image onto the preoperative image. A: Four windows of iPLAN cranial software are indicated. Intraoperative axial T1-weighted image (upper left), intraoperative coronal T2-weighted image (lower left), preoperative axial T1-weighted image (upper right), and preoperative coronal T2-weight image (lower right). All images were fused by the rigid registration algorithm provided by iPLAN and have the same coordinates. The yellow crossbars show the stimulation point. The objects of the FAT, created with preoperative DTI, were overlaid onto preoperative images (upper and lower right). Note that the crossbar on the preoperative images (upper and lower right) seemed to be located inside the tumor, although the tumor had already been resected. B: Extent of the brain shift near the stimulation point was evaluated using anatomical landmarks and measured in x-y-z coordinates (x, mediolateral; y, anteroposterior; z, rostrocaudal). The stimulation point was located at the deep posterolateral aspect of the resection cavity (delineated by the white curved line). Note that the surface and sulci of the frontal lobe (white line) were shifted medially, suggesting that there was an apparent brain shift on the intraoperative image toward the medial direction. The distance between the crossbar and the boundary of the tumor was measured as 7 mm (x axis). A sulcus located in the posterior area of the resection cavity, running slantwise from the medal aspect of the brain in a posterolateral direction, had no apparent shift (0 mm, y axis). The amount of the shift in the z axis was evaluated on the coronal images. Comparison between the bottom of the resection cavity on the intraoperative image and the tumor boundary on the preoperative image (both of them delineated by a yellow line) revealed a 3-mm upward shift in the z-axis direction. C: According to the evaluation above, the amount of the brain shift near the stimulation point was considered as 7 mm medial (x axis) and 3 mm rostral (z axis). The shift in the y axis was 0 mm. Therefore, we concluded that due to the brain shift, the stimulation point on the intraoperative image should be adjusted and moved 7 mm lateral and 3 mm caudal on the preoperative image. Note that the stimulation point is very close to the FAT (red areas).

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    Preoperative coronal MR images in Cases 1–5, with the 3D objects of the FAT, formed by DTI tractography (white areas outlined by black). The yellow crosses show sites that responded positively to electrical stimulation during subcortical mapping in awake surgery. Figure is available in color online only.

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    Subcortical stimulation sites at Tags 12, 13, and 14 from Fig. 4 are indicated on intraoperative T2-weighted images (upper row, yellow crosses). The corresponding points were estimated by correcting the intraoperative brain shift using fused intraoperative and preoperative MR images. The estimated stimulation sites on the preoperative images with the frontal aslant tract are shown in the lower row (yellow crosses). Figure is available in color online only.

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    Case 5. Intraoperative photograph (A), diagram (B), and 3D view of the tractography (C). Cortical mapping showed the primary motor cortex (Tags 1 and 2) and Broca's area (Tags 3, 9, and 7). Subcortical mapping demonstrated positive language symptoms during electrical stimulation at Tags 12, 13, and 14 (yellow arrows). All of these sites were considered adjacent to the frontal aslant tract, based on preoperative DTI examinations and navigation corrected by intraoperative MRI. Anatomical relationships are shown in the diagram (B). The subcortical stimulation sites were overlaid onto a 3D view of the tractography (C), demonstrating that the 3 sites are aligned on the anterior aspect of the object of the frontal aslant tract (pink). green = SLF; purple = IFOF; yellow = corticospinal tract (bilateral).

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