Chinese Verbal Fluency Deficiency in Temporal Lobe Epilepsy with and without Hippocampal Sclerosis: A Multiscale Study

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In this study, a Chinese character version of the phonemic verbal fluency task was tested in patients with temporal lobe epilepsy (TLE) to assess verbal fluency deficiency in TLE with and without hippocampal sclerosis. The results showed activation and deactivation deficiency in both TLE-HS and TLE-NHS, with impaired functional connectivity, degree centrality, and community features in the anterior inferior temporal gyri in TLE-HS but retained or enhanced in TLE-NHS. The study also found that the VFC scores were correlated with semantic fluency in healthy controls and with phonemic fluency in TLE-NHS. Functional connectivity of phonemic circuits was impaired in TLE-HS and enhanced in TLE-NHS, indicating a compensative phonemic searching strategy in TLE-NHS. The neural network classification model reached an area under the curve of 0.90 in diagnosing hippocampal sclerosis. Overall, the study highlights the differences in verbal fluency patterns in TLE with and without hippocampal sclerosis, providing insights into potential clinical applications for the VFC task in TLE.

To test a Chinese character version of the phonemic verbal fluency task in patients with temporal lobe epilepsy (TLE) and assess the verbal fluency deficiency pattern in TLE with and without hippocampal sclerosis, a cross-sectional study was conducted including 30 patients with TLE and hippocampal sclerosis (TLE-HS), 28 patients with TLE and without hippocampal sclerosis (TLE-NHS), and 29 demographically matched healthy controls (HC). Both sexes were enrolled. Participants finished a Chinese character verbal fluency (VFC) task during functional MRI. The activation/deactivation maps, functional connectivity, degree centrality, and community features of the left frontal and temporal regions were compared. A neural network classification model was applied to differentiate TLE-HS and TLE-NHS using functional statistics. The VFC scores were correlated with semantic fluency in HC while correlated with phonemic fluency in TLE-NHS. Activation and deactivation deficiency was observed in TLE-HS and TLE-NHS (p < 0.001, k ≥ 10). Functional connectivity, degree centrality, and community features of anterior inferior temporal gyri were impaired in TLE-HS and retained or even enhanced in TLE-NHS (p < 0.05, FDR-corrected). The functional connectivity was correlated with phonemic fluency (p < 0.05, FDR-corrected). The neural network classification reached an area under the curve of 0.90 in diagnosing hippocampal sclerosis. The VFC task is a Chinese phonemic verbal fluency task suitable for clinical application in TLE. During the VFC task, functional connectivity of phonemic circuits was impaired in TLE-HS and was enhanced in TLE-NHS, representing a compensative phonemic searching strategy applied by patients with TLE-NHS.

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