Convergence of the arcuate fasciculus and third branch of the superior longitudinal fasciculus with direct cortical stimulation–induced speech arrest area in the anterior ventral precentral gyrus

J Neurosurg 139:1140–1151, 2023

The objective was to identify the correspondence between the anterior terminations of the arcuate fasciculus (AF) and third branch of the superior longitudinal fasciculus (SLF-III) and the intraoperative direct cortical electrical stimulation (DCS)–induced speech arrest area.

METHODS The authors retrospectively screened 75 glioma patients (group 1) who received intraoperative DCS mapping in the left dominant frontal cortex. To minimize the influence of tumors or edema, we subsequently selected 26 patients (group 2) with glioma or edema not affecting Broca’s area, the ventral precentral gyrus (vPCG), and the subcortical pathways to generate DCS functional maps and to construct the anterior terminations of AF and SLF-III with tractography. Next, a grid-by-grid pairwise comparison was performed between the fiber terminations and the DCS-induced speech arrest sites to calculate Cohen’s kappa coefficient (κ) in both groups 1 and 2. Finally, the authors also demonstrated the distribution of the AF/SLF-III anterior projection maps obtained in 192 healthy participants (group 3) and subsequently correlated these with the speech arrest sites in group 2 to examine their validity in predicting speech output area.

RESULTS The authors found that speech arrest sites were substantially consistent with SLF-III anterior terminations (group 1, κ = 0.64 ± 0.03; group 2, κ = 0.73 ± 0.05) and moderately consistent with AF (group 1, κ = 0.51 ± 0.03; group 2, κ = 0.49 ± 0.05) and AF/SLF-III complex (group 1, κ = 0.54 ± 0.03; group 2, κ = 0.56 ± 0.05) terminations (all p < 0.0001). The DCS speech arrest sites of the group 2 patients mainly (85.1%) emerged at the anterior bank of the vPCG (vPCGa). In group 3, both terminations of AF and SLF-III converged onto the vPCGa, and their terminations well predicted the DCS speech output area of group 2 (AF, area under the curve [AUC] 86.5%; SLF-III, AUC 79.0%; AF/SLF-III complex, AUC 86.7%).

CONCLUSIONS This study supports the key role of the left vPCGa as the speech output node by showing convergence between speech output mapping and anterior AF/SLF-III connectivity in the vPCGa. These findings may contribute to the understanding of speech networks and could have clinical implications in preoperative surgical planning.

Preservation of language function by mapping the arcuate fasciculus using intraoperative corticocortical evoked potential under general anesthesia in glioma surgery

J Neurosurg 137:1535–1543, 2022

Intraoperative language mapping under general anesthesia is imperative for brain tumor surgery because awake surgery is not always feasible. Monitoring corticocortical evoked potential (CCEP) is known to be a useful method for tracking neuronal connectivity and localizing functional areas. The authors evaluated the clinical benefit of intraoperative CCEP monitoring for language function preservation in patients undergoing glioma surgery.

METHODS Between January 2019 and June 2021, the authors performed a total of 29 consecutive glioma surgeries using CCEP monitoring under general anesthesia because of a risk of speech impairment; these were analyzed. Language area mapping was implemented by the anterior language area to posterior language area CCEP method for arcuate fasciculus mapping, and tumor resection was performed while avoiding the localized language areas. Language function before and after surgery was evaluated by the Controlled Oral Word Association Test (COWAT).

RESULTS Intraoperative CCEP was successfully monitored in 25 patients (86.2%), and a valid signal was undetectable in the other 4 patients. Language function evaluation was possible before and after surgery in a total of 20 patients. Overall, the preservation rate of language function was 65.0%, and the deterioration rate was 35.0% after tumor resection with CCEP monitoring. Among those 8 patients with preoperative COWAT scores ≥ 18, 5 patients (62.5%) successfully preserved their language function, with COWAT scores > 18 after tumor resection. Among the 12 patients with preoperative deteriorated language function (COWAT score < 18), 8 patients (66.7%) showed improvement or preserved language function after surgery.

CONCLUSIONS Intraoperative CCEP monitoring of the arcuate fasciculus is an acceptable technology for the preservation of language function under general anesthesia in glioma surgery in patients in whom awake surgery is not feasible.

Language hemispheric dominance analyzed with magnetic resonance DTI: correlation with the Wada test

J Neurosurg 134:1703–1710, 2021

Language lateralization is a major concern in some patients with pharmacoresistant epilepsy who will face surgery; in these patients, hemispheric dominance testing is essential to avoid further complications. The Wada test is considered the gold standard examination for language localization, but is invasive and requires many human and material resources. Functional MRI and tractography with diffusion tensor imaging (DTI) have demonstrated that they could be useful for locating language in epilepsy surgery, but there is no evidence of the correlation between the Wada test and DTI MRI in language dominance.

METHODS The authors performed a retrospective review of patients who underwent a Wada test before epilepsy surgery at their institution from 2012 to 2017. The authors retrospectively analyzed fractional anisotropy (FA), number and length of fibers, and volume of the arcuate fasciculus and uncinate fasciculus, comparing dominant and nondominant hemispheres.

RESULTS Ten patients with temporal lobe epilepsy were reviewed. Statistical analysis showed that the mean FA of the arcuate fasciculus in the dominant hemisphere was higher than in the nondominant hemisphere (0.369 vs 0.329, p = 0.049). Also, the number of fibers in the arcuate fasciculus was greater in the dominant hemisphere (881.5 vs 305.4, p = 0.003). However, no differences were found in the FA of the uncinate fasciculus or number of fibers between hemispheres. The length of fibers of the uncinate fasciculus was longer in the dominant side (74.4 vs 50.1 mm, p = 0.05). Volume in both bundles was more prominent in the dominant hemisphere (12.12 vs 6.48 cm3, p = 0.004, in the arcuate fasciculus, and 8.41 vs 4.16 cm3, p = 0.018, in the uncinate fasciculus). Finally, these parameters were compared in patients in whom the seizure focus was situated in the dominant hemisphere: FA (0.37 vs 0.30, p = 0.05), number of fibers (114.4 vs 315.6, p = 0.014), and volume (12.58 vs 5.88 cm3, p = 0.035) in the arcuate fasciculus were found to be statistically significantly higher in the dominant hemispheres. Linear discriminant analysis of FA, number of fibers, and volume of the arcuate fasciculus showed a correct discrimination in 80% of patients (p = 0.024).

CONCLUSIONS The analysis of the arcuate fasciculus and other tract bundles by DTI could be a useful tool for language location testing in the preoperative study of patients with refractory epilepsy.

Symmetry of the arcuate fasciculus and its impact on language performance of patients with brain tumors in the language-dominant hemisphere

J Neurosurg 127:1407–1416, 2017

Cerebral damage in frontal, parietal, and temporal brain areas and, probably more importantly, their interconnections can lead to deficits in language. However, neural plasticity and repair allow the brain to partly compensate for neural injury, mediated by both functional and structural changes. In this study, the authors sought to systematically investigate the relationship between language performance in brain tumor patients and structural perisylvian pathways (i.e., the arcuate fasciculus [AF]) using probabilistic fiber tracking on diffusion tensor imaging. The authors used a previously proposed model in which the AF is divided into anterior, long, and posterior segments. The authors hypothesized that right-handed patients with gliomas in the language-dominant (left) hemisphere would benefit from a more symmetrical or right-lateralized language pathway in terms of better preservation of language abilities. Furthermore, they investigated to what extent specific tumor characteristics, including proximity to the AF, affect language outcome in such patients.

METHODS Twenty-seven right-handed patients (12 males and 15 females; mean age 52 ± 16 years) with 11 low-grade and 16 high-grade gliomas of the left hemisphere underwent 3-T diffusion-weighted MRI (30 directions) and language assessment as part of presurgical planning. For a systematic quantitative evaluation of the AF, probabilistic fiber tracking with a 2 regions of interest approach was carried out. Volumes of the 3 segments of both hemispheric AFs were evaluated by quantifying normalized and thresholded pathways. Resulting values served to generate the laterality index of the AFs.

RESULTS Patients without language deficits tended to have an AF that was symmetric or lateralized to the right, whereas patients with deficits in language significantly more often demonstrated a left-lateralized posterior segment of the AF. Patients with high-grade gliomas had more severe language deficits than those with low-grade gliomas. Backward logistic regression revealed the laterality index of the posterior AF segment and tumor grade as the only independent statistically significant predictors for language deficits in this cohort.

CONCLUSIONS In addition to the well-known fact that tumor entity influences behavioral outcome, the authors’ findings suggest that the right homologs of structural language-associated pathways could be supportive for language function and facilitate compensation mechanisms after brain damage in functionally eloquent areas. This further indicates that knowledge about preoperative functional redistribution (identified by neurofunctional imaging) increases the chance for total or near-total resections of tumors in eloquent areas. In the future, longitudinal studies with larger groups are mandatory to overcome the methodological limitations of this cross-sectional study and to map neuroplastic changes associated with language performance and rehabilitation in brain tumor patients.

 

Fiber tracts of the dorsal language stream in the human brain

Fiber tracts of the dorsal language stream in the human brain

J Neurosurg 124:1396–1405, 2016

The aim of this study was to examine the arcuate (AF) and superior longitudinal fasciculi (SLF), which together form the dorsal language stream, using fiber dissection and diffusion imaging techniques in the human brain.

Methods Twenty-five formalin-fixed brains (50 hemispheres) and 3 adult cadaveric heads, prepared according to the Klingler method, were examined by the fiber dissection technique. The authors’ findings were supported with MR tractography provided by the Human Connectome Project, WU-Minn Consortium. The frequencies of gyral distributions were calculated in segments of the AF and SLF in the cadaveric specimens.

Results The AF has ventral and dorsal segments, and the SLF has 3 segments: SLF I (dorsal pathway), II (middle pathway), and III (ventral pathway). The AF ventral segment connects the middle (88%; all percentages represent the area of the named structure that is connected to the tract) and posterior (100%) parts of the superior temporal gyri and the middle part (92%) of the middle temporal gyrus to the posterior part of the inferior frontal gyrus (96% in pars opercularis, 40% in pars triangularis) and the ventral premotor cortex (84%) by passing deep to the lower part of the supramarginal gyrus (100%). The AF dorsal segment connects the posterior part of the middle (100%) and inferior temporal gyri (76%) to the posterior part of the inferior frontal gyrus (96% in pars opercularis), ventral premotor cortex (72%), and posterior part of the middle frontal gyrus (56%) by passing deep to the lower part of the angular gyrus (100%).

Conclusions This study depicts the distinct subdivision of the AF and SLF, based on cadaveric fiber dissection and diffusion imaging techniques, to clarify the complicated language processing pathways.

Three-Dimensional Topographic Fiber Tract Anatomy of the Cerebrum

Three-Dimensional Topographic Fiber Tract Anatomy of the Cerebrum

Neurosurgery 11:274–305, 2015

The fiber tracts of the cerebrum may be a more important determinant of resection limits than the cortex. Better knowledge of the 3-dimensional (3-D) anatomic organization of the fiber pathways is important in planning safe and accurate surgery for lesions within the cerebrum.

OBJECTIVE: To examine the topographic anatomy of fiber tracts and subcortical gray matter of the human cerebrum and their relationships with consistent cortical, ventricular, and nuclear landmarks.

METHODS: Twenty-five formalin-fixed human brains and 4 whole cadaveric heads were examined by fiber dissection technique and ·6 to ·40 magnification. The fiber tracts and central core structures, including the insula and basal ganglia, were examined and their relationships captured in 3-D photography. The depth between the surface of the cortical gyri and selected fiber tracts was measured.

RESULTS: The topographic relationships of the important association, projection, and commissural fasciculi within the cerebrum and superficial cortical landmarks were identified. Important landmarks with consistent relationships to the fiber tracts were the cortical gyri and sulci, limiting sulci of the insula, nuclear masses in the central core, and lateral ventricles. The fiber tracts were also organized in a consistent pattern in relation to each other. The anatomic findings are briefly compared with functional data from clinicoradiological analysis and intraoperative stimulation of fiber tracts.

CONCLUSION: An understanding of the 3-D anatomic organization of the fiber tracts of the brain is essential in planning safe and accurate cerebral surgery.

Arcuate fasciculus in brain tumor surgery

J Neurosurg 117:839–843, 2012 

Disturbance of the arcuate fasciculus in the dominant hemisphere is thought to be associated with language- processing disorders, including conduction aphasia. Although the arcuate fasciculus can be visualized in vivo with diffusion tensor imaging (DTI) tractography, its involvement in functional processes associated with language has not been shown dynamically using DTI tractography. In the present study, to clarify the participation of the arcuate fasciculus in language functions, postoperative changes in the arcuate fasciculus detected by DTI tractography were evaluated chronologically in relation to postoperative changes in language function after brain tumor surgery.

Methods. Preoperative and postoperative arcuate fasciculus area and language function were examined in 7 right-handed patients with a brain tumor in the left hemisphere located in proximity to part of the arcuate fasciculus. The arcuate fasciculus was depicted, and its area was calculated using DTI tractography. Language functions were measured using the Western Aphasia Battery (WAB).

Results. After tumor resection, visualization of the arcuate fasciculus was increased in 5 of the 7 patients, and the total WAB score improved in 6 of the 7 patients. The relative ratio of postoperative visualized area of the arcuate fasciculus to preoperative visualized area of the arcuate fasciculus was increased in association with an improvement in postoperative language function (p = 0.0039).

Conclusions. The role of the left arcuate fasciculus in language functions can be evaluated chronologically in vivo by DTI tractography after brain tumor surgery. Because increased postoperative visualization of the fasciculus was significantly associated with postoperative improvement in language functions, the arcuate fasciculus may play an important role in language function, as previously thought. In addition, postoperative changes in the arcuate fasciculus detected by DTI tractography could represent a predicting factor for postoperative language-dependent functional outcomes in patients with brain tumor.

Correlation between language function and the left arcuate fasciculus detected by diffusion tensor imaging tractography after brain tumor surgery

J Neurosurg 117:839–843, 2012

Disturbance of the arcuate fasciculus in the dominant hemisphere is thought to be associated with language-processing disorders, including conduction aphasia. Although the arcuate fasciculus can be visualized in vivo with diffusion tensor imaging (DTI) tractography, its involvement in functional processes associated with language has not been shown dynamically using DTI tractography. In the present study, to clarify the participation of the arcuate fasciculus in language functions, postoperative changes in the arcuate fasciculus detected by DTI tractography were evaluated chronologically in relation to postoperative changes in language function after brain tumor surgery.

Methods. Preoperative and postoperative arcuate fasciculus area and language function were examined in 7 right-handed patients with a brain tumor in the left hemisphere located in proximity to part of the arcuate fasciculus. The arcuate fasciculus was depicted, and its area was calculated using DTI tractography. Language functions were measured using the Western Aphasia Battery (WAB).

Results. After tumor resection, visualization of the arcuate fasciculus was increased in 5 of the 7 patients, and the total WAB score improved in 6 of the 7 patients. The relative ratio of postoperative visualized area of the arcuate fasciculus to preoperative visualized area of the arcuate fasciculus was increased in association with an improvement in postoperative language function (p = 0.0039).

Conclusions. The role of the left arcuate fasciculus in language functions can be evaluated chronologically in vivo by DTI tractography after brain tumor surgery. Because increased postoperative visualization of the fasciculus was significantly associated with postoperative improvement in language functions, the arcuate fasciculus may play an important role in language function, as previously thought. In addition, postoperative changes in the arcuate fasciculus detected by DTI tractography could represent a predicting factor for postoperative language-dependent functional outcomes in patients with brain tumor.