Patients
Between January 2014 and December 2019, a total of 65 consecutive patients who underwent craniotomy for resection of gliomas located in the left temporal or parietal lobe were recruited in our hospital. Among them, 51 patients were followed up after surgery until 6 months postoperatively (Supplementary Information 1), and 46 patients underwent awake craniotomy (Supplementary Information 2). Written informed consent was obtained from the individual(s) or next of kin for the publication of any potentially identifiable images or data included in this article. This study was performed according to the guidelines of the Internal Review Board of Kanazawa University and approved by the medical ethics committee of Kanazawa University (Approval number: 3293).
Neuropsychological assessment
Before and after surgery, patients underwent language assessment tests, such as the Western Aphasia battery (WAB; Japanese version), conducted by a well-experienced speech specialist and an occupational therapist (OH and RN, respectively). The WAB test consists of eight subcategories (spontaneous speech, auditory comprehension, naming, repetition, reading, wiring, praxis, and construction) (Kertesz 1982; Shewan 1986). In particular, reading skill was evaluated for both kanji and kana in the WAB test. On the basis of the scores of these subcategories, the aphasia quotient (AQ), an individual parameter for the severity of aphasia, was calculated. Patients with severe aphasia, including other language disorders, were excluded from our study. Subsequently, all patients were categorized by the speech specialist and occupational therapist (OH and RN) into three groups as follows: no dyslexia, kanji dyslexia, and kana dyslexia.
Magnetic resonance imaging (MRI) and postprocessing
Structural MRI was performed as part of standard perioperative care. Diffusion-weighted MRI (DW-MRI) was performed using a 3.0 Tesla MRI scanner (Signa™ Excite HDx 3.0T, General Electric Healthcare, Little Chalfont, UK) under the same conditions as previously reported (Kinoshita et al. 2016). A series of axial diffusion-weighted images (b-value: 0 to 1,000 s/mm2) with a diffusion-sensitizing gradient along 30 directions were obtained. Other parameters for this study were as follows: repetition time = 1,4000 ms, echo time = 69.6 ms, number of extractions = 2, 60 axial slices with slice thickness = 2.5 mm with no interslice gap, and field of view = 220 × 220 mm with a matrix = 88 × 88, resulting in an effective resolution of 2.5-mm3 isotropic voxels. The DW-MRI data were transferred to a workstation using iPlan Cranial 3.0 software (Brainlab, Feldkirchen, Germany), and white-matter tracts of the AF, posterior SLF, and ILF were selected and visualized. All the fiber tracts were constructed with fiber propagation (fractional anisotropy threshold > 0.18). To reconstruct each fiber tract, regions of interest were determined manually by referring to the diffusion tensor imaging tractography atlas and previous reports (Catani et al. 2002; Kinoshita et al. 2016; Makris et al. 2005). Each MRI was converted to the Montreal Neurological Institute (MNI) template using SPM12 (http://www.fil.ion.ucl.ac.uk/spm/software/spm12/), which was implemented in the MATLAB environment (http://www.mathworks.com/products/matlab/). The resection cavities were reconstructed manually using MRIcron software (http://www.mccauslandcenter.sc.edu/mricro/mricron/). We investigated the regions showing maximum overlap in kanji or kana dyslexia and identified the regions that overlapped in all cases of postoperative kanji or kana dyslexia on the three-dimensional (3D) MNI template.
Procedure for identification of overlapping positive mapping points
The procedure for identification of overlapping positive mapping points was the same as that described in previous reports (Nakajima et al. 2020a). First, subcortical positive mapping points were plotted on postoperative 3D T1 MR images while referring to the operative findings and intraoperative records with iPlan Cranial 3.0 software (BrainLab). The locations of these mapping points were confirmed by determining their spatial relationships to anatomical landmarks: gyri, sulci, artery, and lateral ventricles. We also checked the mapping points on 2D axial, sagittal, and coronal MRI images. These procedures were first performed by ST and inspected systematically by RN and MK.
Procedure for awake craniotomy
Using the same procedure as that described in previous reports, all 46 patients underwent awake craniotomy using the “Asleep-Awake-Asleep” technique, with cortical and subcortical brain mapping achieved by DES using a bipolar electrode with 5-mm spaced tips (Duffau et al. 2002). A biphasic current was used with a pulse frequency of 60 Hz and amplitude depending on cortical mapping stimulation (3–6 mA). Surgical resection was stopped when DES revealed specific neurological findings and disorders during task execution, including picture-naming tasks and alternate reading tasks for kana or kanji (Supplementary Information 3 and 4, Video). All positive mapping sites were labeled by number tags, and intraoperative photographs were obtained. We investigated the relationship between the subcortical DES mapping points and the intraoperative kanji or kana dyslexia.
The operative view and intraoperative neuropsychological assessments were recorded using a video camera. Intraoperative tasks for glioma patients were selected depending on their social background, motivation, and tumor location. To address the oncological priorities in these patients, we performed surgical resection as follows: first, we resected the enhanced lesion of the tumor, which was followed by extended resection with the appropriate intraoperative assessments (Esquenazi et al. 2017). In particular, the typical measurement for aphasia in Japanese was based on naming tasks. Intraoperatively, we showed slides that alternately indicated kana and kanji words every 4 seconds and evaluated whether the patients could read these words correctly. We identified the following situations as incorrect reading: no response, sequential reading, and phonetic error.