Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy

Abstract

Background and Objectives:In medically refractory temporal lobe epilepsy (TLE), 30-50% of patients experience substantial language decline following resection in the language dominant hemisphere. Here, we investigate the contribution of white matter fiber bundle damage to language change at 3- and 12-months after surgery.Methods:We studied 127 patients who underwent TLE surgery from 2010–2019. Neuropsychological testing included picture naming, semantic, and phonemic verbal fluency, performed pre-operatively, 3- and 12-months post-operatively. Outcome was assessed using reliable change index (RCI; clinically significant decline) and change across timepoints (post- minus pre-operative scores).Functional MRI was used to determine language lateralization. The arcuate (AF), inferior fronto-occipital (IFOF), inferior longitudinal, middle longitudinal (MLF), and uncinate fasciculi were mapped using diffusion MRI probabilistic tractography. Resection masks, drawn comparing co-registered pre- and post-operative T1 MRI scans, were used as exclusion regions on pre-operative tractography to estimate the percentage of pre-operative tracts transected in surgery. Chi-squared assessments evaluated the occurrence of RCI-determined language decline. Independent samples T-tests and MM-estimator robust regressions were used to assess the impact of clinical factors and fiber transection on RCI and change outcomes, respectively.Results:Language dominant and non-dominant resections were treated separately for picture naming, as post-operative outcomes were significantly different between these groups. In language dominant hemisphere resections, greater surgical damage to the AF and IFOF was related to RCI-decline at 3 months. Damage to the inferior frontal sub-fasciculus of the IFOF was related to change at 3 months. In language non-dominant hemisphere resections, increased MLF resection was associated with RCI-decline at 3 months, and damage to the anterior sub-fasciculus was related to change at 3 months.Language dominant and non-dominant resections were treated as one cohort for semantic and phonemic fluency, as there were no significant differences in post-operative decline between these groups. Post-operative seizure freedom was associated with an absence of significant language decline 12 months after surgery for semantic fluency.Discussion:We demonstrate a relationship between fiber transection and naming decline after temporal lobe resection. Individualized surgical planning to spare white matter fiber bundles could help to preserve language function after surgery.

The impact of temporal lobe epilepsy surgery on picture naming and its relationship to network metric change

“…Reduced white matter connectivity between these regions could impair visual recognition and memory retrieval. We can infer that this supports our previous research which linked the integrity of the inferior-fronto-occipital fasciculus (IFOF), which interconnects these regions, to picture naming decline at 3 months post-injury ( Binding et al, 2023 ). While our previous analysis did not find a relationship between IFOF integrity and naming decline at 12 months, the IFOF encapsulates cortical connections to many regions beyond the two regions we included in our analysis.…”

“…Our study found that estimated changes in all graph theory metrics (i.e., clustering coefficient, betweenness centrality, and strength) and clinical factors were able to classify decline in picture naming at 3 months after ATLR with an AUC of 0.89. Previous research showed that language function dips immediately after surgery followed by some patients improving ( Binding et al, 2023 ). As such, our results suggest that all clustering coefficient, betweenness centrality, strength, and clinical factors play a role in the preparedness of the brain to a temporal lobe resection.…”

“…White matter fibres are anatomically arranged in fibre bundles. Recent work has demonstrated that transection of specific fibre bundles within the temporal lobe contributes to picture naming decline ( Binding et al, 2023 , Herbet et al, 2016 ). Fibre bundle analysis, however, is limited by our understanding of white matter fibre anatomy and function.…”

Non-Invasive Brain Mapping Localizes Essential Language Function in Surgical Glioma Patients

“…Multiple previous studies have predicted language outcomes with preoperative imaging while others have documented associations between resections and postoperative language decline. [19][20][21][22][23][24][25] However, in our view, this study has unique clinical value. Here we report novel data that can directly inform operative decisions by predicting the long-term functional impact of individual tumor-removal strategies with strong accuracy (>90%).…”

Advancements in Diffusion MRI Tractography for Neurosurgery

“…Nonetheless, the prediction of postoperative language dysfunction is crucial because patients whose language-dominant hemispheres are resected have a substantial risk (ranging from 30% to 50%) of experiencing a decline in their language-related function after the surgical procedure. For instance, Binding et al 64 used probabilistic tractography to map language-related white matter tracts (such as the AF, uncinate fasciculus, inferior longitudinal fasciculus, middle longitudinal fasciculus, and inferior fronto-occipital fasciculus) in 127 patients undergoing TLE surgery to explore the correlation between postoperative language function assessment and the percentage of white matter tracts impaired by the surgery. According to their findings, in language-dominant hemispherectomy, the greater the surgical damage to the AF and inferior fronto-occipital fasciculus, the worse the language function at 3 months.…”