White-matter pathways and semantic processing: intrasurgical and lesion-symptom mapping evidence

• Published in: NeuroImage clinical Vol. 22; p. 101704
• Main Authors: Sierpowska, Joanna, Gabarrós, Andreu, Fernández-Coello, Alejandro, Camins, Àngels, Castañer, Sara, Juncadella, Montserrat, François, Clément, Rodríguez-Fornells, Antoni
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier 01-01-2019
• Subjects: Adolescent; Adult; Aged; Brain - physiology; Brain Mapping - methods; Brain Neoplasms - surgery; Cognitive science; Comprehension - physiology; Electric Stimulation; Female; Humans; Intraoperative Neurophysiological Monitoring - methods; Language; Linguistics; Male; Middle Aged; Neural Pathways - physiology; Neuroscience; Neurosurgical Procedures - methods; Psychology; Regular; Semantics; White Matter - physiology; Young Adult; Semantic processing; Dual stream models for language processing; Diffusion tensor imaging (DTI); ESM = electrical stimulation mapping; Voxel lesion-symptom mapping (VLSM); electrical stimulation mapping
• ISSN: 2213-1582; 2213-1582
• DOI: 10.1016/j.nicl.2019.101704

In the present study, we aimed to test the association between the correct function of the left ventral white matter pathways and semantic processing (dual stream models for language processing, Hickok & Poeppel, 2004), using a new set of language tasks during intraoperative electrical stimulation at white matter level. Additionally, we evaluated brain regions needed for correct performance on the different semantic tasks using lesion-symptom analyses (voxel lesion-symptom mapping and track-wise lesion analysis) in a sample of 62 candidates for the awake brain surgery. We found that electrical stimulation in the vicinity of the inferior longitudinal and inferior fronto-occipital fasciculi disturbed performance on semantic processing tasks. Individuals presented with significantly more semantic paraphasias during brain tumor resection than during the electrical stimulation at the cortex level. Track-wise analyses confirmed the role of these left ventral pathways in semantic processing: a significant relationship was observed between the probability of inferior fronto-occipital fasciculus disconnection/damage and the semantic matching tasks, as well as the number of semantic paraphasias in naming. Importantly, the same analyses for the total score of the Boston Naming Test confirmed significant relationships between this test score and the integrity of the inferior fronto-occipital, inferior longitudinal and uncinate fasciculi. This was further supported by the results of VLSM analyses showing a significant relationship between BNT and the presence of lesion within left middle and inferior temporal gyri. The present findings provide new intraoperative evidence for the role of the white-matter ventral pathways in semantic processing, while at the same time emphasizing the need to include a broader assessment of semantic-conceptual aspects during the awake neurosurgical intervention. This approach will ensure better preservation of functional tissue in the tumoral vicinity and therefore substantially diminish post-surgical language impairments.