ObjectNavigated transcranial magnetic stimulation (nTMS) combined with diffusion tensor imaging (DTI) is used preoperatively in patients with eloquent-located brain lesions and allows analyzing non-invasively the spatial relationship between the tumor and functional areas (e.g. the motor cortex and the corticospinal tract [CST]). In this study, we examined the diffusion parameters FA (fractional anisotropy) and ADC (apparent diffusion coefficient) within the CST in different locations and analyzed their interrater reliability and usefulness for predicting the patients' motor outcome with a precise approach of specific region of interest (ROI) seeding based on the color-coded FA-map.MethodsProspectively collected data of 30 patients undergoing bihemispheric nTMS mapping followed by nTMS-based DTI fiber tracking prior to surgery of motor eloquent high-grade gliomas were analyzed by 2 experienced and 1 unexperienced examiner. The following data were scrutinized for both hemispheres after tractography based on nTMS-motor positive cortical seeds and a 2nd region of interest in one layer of the caudal pons defined by the color-coded FA-map: the pre- and postoperative motor status (day of discharge und 3 months), the closest distance between the tracts and the tumor (TTD), the fractional anisotropy (FA) and the apparent diffusion coefficient (ADC). The latter as an average within the CST as well as specific values in different locations (peritumoral, mesencephal, pontine).ResultsLower average FA-values within the affected CST as well as higher average ADC-values are significantly associated with deteriorated postoperative motor function (p = 0.006 and p = 0.026 respectively). Segmental analysis within the CST revealed that the diffusion parameters are especially disturbed on a peritumoral level and that the degree of their impairment correlates with motor deficits (FA p = 0.065, ADC p = 0.007). No significant segmental variation was seen in the healthy hemisphere. The interrater reliability showed perfect agreement for almost all analyzed parameters.ConclusionsAdding diffusion weighted imaging derived information on the structural integrity of the nTMS-based tractography results improves the predictive power for postoperative motor outcome. Utilizing a second subcortical ROI which is specifically seeded based on the color-coded FA map increases the tracking quality of the CST independently of the examiner's experience. Further prospective studies are needed to validate the nTMS-based prediction of the patient's outcome.

In preoperative planning for neurosurgery, both anatomical (diffusion imaging tractography) and functional tools (MR-navigated transcranial magnetic stimulation) are increasingly used to identify and preserve eloquent language structures specific to individuals. Using these tools in healthy adults shows that speech production errors occur mainly in perisylvian cortical sites that correspond with subject-specific terminations of the major language pathway, the arcuate fasciculus. It is not clear whether this correspondence remains in oncological patients with altered tissue. We studied a heterogeneous cohort of thirty patients (fourteen male, mean age 44), undergoing a first or second surgery for a left hemisphere brain tumour in a language-eloquent region, to test whether speech production errors induced by preoperative transcranial magnetic stimulation had consistent anatomical correspondence with the arcuate fasciculus. We used navigated repetitive transcranial magnetic stimulation during picture naming and recorded different perisylvian sites where transient interference to speech production occurred. Spherical deconvolution diffusion imaging tractography was performed to map the direct fronto-temporal and indirect (fronto-parietal and parieto-temporal) segments of the arcuate fasciculus in each patient. Speech production errors were reported in all patients when stimulating the frontal lobe, and in over 90% of patients in the parietal lobe. Errors were less frequent in the temporal lobe (54%). In all patients, at least one error site corresponded with a termination of the arcuate fasciculus, particularly in the frontal and parietal lobes, despite distorted anatomy due to a lesion and/or previous resection. Our results indicate that there is strong correspondence between terminations of the arcuate fasciculus and speech errors. This indicates that white matter anatomy may be a robust marker for identifying functionally eloquent cortex, particularly in the frontal and parietal lobe. This knowledge may improve targets for preoperative mapping of language in the neurosurgical setting.

The arcuate fasciculus has been considered a major dorsal fronto-temporal white matter pathway linking frontal language production regions with auditory perception in the superior temporal gyrus, the so-called Wernicke’s area. In line with this tradition, both historical and contemporary models of language function have assigned primacy to superior temporal projections of the arcuate fasciculus. However, classical anatomical descriptions and emerging behavioural data are at odds with this assumption. On one hand, fronto-temporal projections to Wernicke’s area may not be unique to the arcuate fasciculus. On the other hand, dorsal stream language deficits have been reported also for damage to middle, inferior and basal temporal gyri which may be linked to arcuate disconnection. These findings point to a reappraisal of arcuate projections in the temporal lobe. Here, we review anatomical and functional evidence regarding the temporal cortical terminations of the left arcuate fasciculus by incorporating dissection and tractography findings with stimulation data using cortico-cortical evoked potentials and direct electrical stimulation mapping in awake patients. Firstly, we discuss the fibers of the arcuate fasciculus projecting to the superior temporal gyrus and the functional rostro-caudal gradient in this region where both phonological encoding and auditory-motor transformation may be performed. Caudal regions within the temporoparietal junction may be involved in articulation and associated with temporoparietal projections of the third branch of the superior longitudinal fasciculus, while more rostral regions may support encoding of acoustic phonetic features, supported by arcuate fibres. We then move to examine clinical data showing that multimodal phonological encoding is facilitated by projections of the arcuate fasciculus to superior, but also middle, inferior and basal temporal regions. Hence, we discuss how projections of the arcuate fasciculus may contribute to acoustic (middle-posterior superior and middle temporal gyri), visual (posterior inferior temporal/fusiform gyri comprising the visual word form area) and lexical (anterior-middle inferior temporal/fusiform gyri in the basal temporal language area) information in the temporal lobe to be processed, encoded and translated into a dorsal phonological route to the frontal lobe. Finally, we point out surgical implications for this model in terms of the prediction and avoidance of neurological deficit.