Localization Patterns of Language Errors in the Brain during Direct Electrical Stimulation: A Systematic Review

EasyChair Preprint № 6479 Localization Patterns of Language Errors in the Brain during Direct Electrical Stimulation: A Systematic Review Ellen Collee, Arnaud Vincent, Evy Visch-Brink, Elke De Witte, Clemens Dirven and Djaina Satoer EasyChair preprints are intended for rapid dissemination of research results and are integrated with the rest of EasyChair. August 30, 2021 Localization Patterns of Language Errors in the Brain during Direct Electrical Stimulation: A Systematic Review E. Collée1, A. Vincent1, E. Visch-Brink1, E. De Witte1, C. Dirven1, D. Satoer1 1 Department of Neurosurgery, Erasmus MC University Medical Centre, Rotterdam, the Netherlands *E. Collée, k.collee@erasmusmc.nl Introduction Awake craniotomy with direct electrical stimulation (DES) is the standard treatment for patients with eloquent area gliomas. Language errors are detected with DES and indicate functional boundaries that need to be maintained during tumor resection to preserve quality of life. Traditionally, counting and object naming were used during DES. The Dutch Linguistic Intraoperative Protocol (DuLIP, De Witte et al., 2015) was the first linguistic test-battery with tasks at different linguistic modalities and levels (production, comprehension, reading, phonology, semantics, syntax) divided into cortico-subcortical areas. The DuLIP model was based on the (limited) available literature and knowledge at the time. As much has been done since, the model needs to be updated. We investigate the localization patterns of different speech/language errors during awake craniotomy. Methods A systematic review was conducted and 102 studies were included reporting on speech arrests and specific speech/language errors and their corresponding brain locations during awake glioma craniotomy with DES. Language errors were counted and categorized in modalities or levels: speech errors (speech arrest, dysarthria/anarthria, verbal apraxia), speech initiation difficulty, semantic errors, phonemic errors, syntactic errors, reading errors and writing errors. Results A wide distribution of brain locations (hemispheres combined) for all speech/language errors (n=930) was found with different patterns. Cortically, errors occurred most often in the precentral gyrus (22%), while subcortically at the inferior fronto-occipital fascicle (IFOF: 11%). Localization patterns for specific speech/language errors were also found: speech errors (n=388)-precentral gyrus (43%), inferior frontal gyrus (9%), postcentral gyrus (4%), frontal aslant/striatal tract (3%); speech initiation difficulty (n=9)-frontal aslant tract (33%), frontal striatal tract (22%); supplementary motor area (22%); semantic errors (n=128)-IFOF (57%), superior temporal gyrus (9%); phonemic errors (n=115)-arcuate fascicle (52%), superior longitudinal fascicle (10%), uncinate fascicle (3%); syntactic errors (n=15)-inferior frontal gyrus (27%); reading errors (n=25)-temporal lobe (48%), inferior longitudinal fascicle (32%) and writing errors (n=7)-superior parietal gyrus (71%). Conclusions This is the first systematic review on the localization of speech/language errors during awake craniotomy. The localization of most speech/language errors are consistent with the assumed functionality of those brain locations as presented in the DuLIP model. However, additional locations for articulation/motor speech, phonology, reading and writing were found and are added to the model, as shown in blue italic print (Table 1). Importantly, many articles exclusively administered object naming, which is not always sensitive enough to find deficits at different linguistic modalities. Subsequently, errors may have been missed. Therefore, we suggest to always use multiple language tests tapping into different modalities and/or levels. Next to DuLIP, various options are available (e.g. Dragoy et al., 2020; Ohlerth et al., 2020, Rofes et al., 2017; Sierpowska et al., 2017). The updated DULIP model should be considered for future selection of perioperative language tasks to improve language testing/monitoring, which may pave the way to a better postoperative language outcome. The possible relation between different intraoperative speech/language errors and postoperative language outcome has yet to be determined. References De Witte, E., Satoer, D., Robert, E., Colle, H., Verheyen, S., Visch-Brink, E., & Mariën, P. (2015). The Dutch linguistic intraoperative protocol: a valid linguistic approach to awake brain surgery. Brain and Language, 140, 35-48. Dragoy, O., Zyryanov, A., Bronov, O., Gordeyeva, E., Gronskaya, N., Kryuchkova, O., ... & Pedyash, N. (2020). Functional linguistic specificity of the left frontal aslant tract for spontaneous speech fluency: Evidence from intraoperative language mapping. Brain and Language, 208, 104836. Ohlerth, A. K., Valentin, A., Vergani, F., Ashkan, K., & Bastiaanse, R. (2020). The verb and noun test for peri-operative testing (VAN-POP): standardized language tests for navigated transcranial magnetic stimulation and direct electrical stimulation. Acta Neurochirurgica, 162(2), 397-406. Rofes, A., Mandonnet, E., Godden, J., Baron, M. H., Colle, H., Darlix, A., ... & Wager, M. (2017). Survey on current cognitive practices within the European Low-Grade Glioma Network: towards a European assessment protocol. Acta neurochirurgica, 159(7), 1167-1178. Sierpowska, J., Gabarrós, A., Fernandez-Coello, A., Camins, À., Castañer, S., Juncadella, M., ... & Rodríguez-Fornells, A. (2017). Words are not enough: nonword repetition as an indicator of arcuate fasciculus integrity during brain tumor resection. Journal of Neurosurgery, 126(2), 435-445. Van Ierschot, F., Bastiaanse, R., & Miceli, G. (2018). Evaluating spelling in glioma patients undergoing awake surgery: a systematic review. Neuropsychology review, 28(4), 470495. Table 1. Suggestions for modification of the Dutch Linguistic Intraoperative Protocol (DuLIP) model for cortical and subcortical brain locations and their corresponding functions and tasks. Brain location Function(s) Frontal regions Inferior frontal gyrus Articulatory (writing) Intraoperative language tasks from DuLIP processing, syntax, Verbal diadochokinesis, repetition, verb generation, action naming Posterior midfrontal gyrus Action naming, (writing) Action naming Supplementary motor area (posterior superior frontal gyrus) Precentral gyrus Language initiation Motor network Sentence completion (close and broad context), fluency Repetition, verbal diadochokinesis Semantics, naming living objects, auditory comprehension Semantic odd picture out, semantic judgement, object naming Phonological network Phonological judgement Anterior middle temporal gyrus Lexical interface, naming non-living objects, reading Famous face naming, reading Semantic judgement, object naming, reading Naming, reading Parietal Regions Supramarginal gyrus Reading, naming, semantics Reading, sentence completion, semantic association, naming Angular gyrus (ANG) Reading, writing Reading, sentence completion Postcentral gyrus Articulatory programming/motor speech Writing Verbal diadochokinesis Initiation of speech, motor speech Phonology Fluency, sentence completion, verbal diadochokinesis Semantic association, semantic odd word/picture out, semantic judgement Reading, sentence completion, naming, repetition Verbal diadochokinesis, repetition, phonological odd word out Repetition, phonological odd word out Famous face naming, semantics, phonology Motor speech Naming, semantic odd picture out, repetition Verbal diadochokinesis, repetition Temporal Regions Posterior superior temporal gyrus Middle posterior superior temporal sulcus Middle inferior temporal gyrus Superior parietal gyrus Subcortical pathways Subcallosal fascicle (= frontal striatal tract), frontal aslant tract Inferior fronto-occipital fascicle Semantics, reading, judgement Inferior longitudinal fascicle Reading, phonology, semantics Superior longitudinal (arcuate fascicle) Arcuate fascicle Articulatory processing, phonology Uncinate fascicle Corticospinal tract fascicle Writing (e.g. Van Ierschot et al., 2018) This table is taken and adjusted from De Witte et al. (2015). Black print is from the original model, blue italic print are additions from the authors based on the data in this review.