Atypical electroencephalographic language lateralization in temporal lobe epilepsy as revealed by fast periodic visual stimulation

Rationale : Language functions are left lateralized in the majority of the healthy population. However, this dominance of the left hemisphere is not systematic and presents inter-individual variability, underlining the importance of developing non-invasive sensitive, objective and reliable measures at the individual level. This is especially relevant in pa-tients with drug-resistant left temporal lobe epilepsy (LTLE) who may present atypical language lateralization and frequent language disorders. The assessment of this atypical representation is crucial to understand and prevent cognitive language disorders in TLE patients who are candidates for cortical surgery. Unfortunately, there are methodological and practical limitations in using neuroimaging techniques and linguistic tasks to determine language lateralization, particularly in this population.
Methods: Here we used a fast periodic visual stimulation approach coupled with high-density (64 channels) electroencephalogram (FPVS-EEG) providing objective and sensi-tive measurement of language lateralization across three visual word stimulation para-digms. LTLE patients (N=18) and matched healthy adults (18) were presented with 1) written words embedded periodically in rapidly presented variable nonwords and pseudo-letters (Lochy et al., 2015), 2) words of the same semantic category (i.e., animals) em-bedded in words of another category (i.e., cities) (Volfart et al., 2021) and 3) celebrity names embedded in unknown names (unpublished). All three paradigms were adminis-tered in total in only 15 minutes, with rapid objective identification and quantification of lexico-semantic markers in the EEG frequency-domain (e.g., Rossion et al., 2020).
Results : While category-selective periodic neural responses over the occipito-temporal cortex were all left lateralized in healthy controls, we report atypical lateralization at the group level in LTLE, characterized by shifted lateralization (i.e., to the right occipito-temporal) and/or bilateral lateralization in the three paradigms. Although this atypical lateralization is consistent with previous studies, different patterns are found across individ-ual patients, showing that this atypical language representation is not systematic. Further analysis is needed to understand the sources of these inter-individual variabilities (e.g., duration of disease, handedness).
Conclusions : Atypical hemispheric lateralization of lexico-semantic language processes in LTLE can be rapidly measured with FPVS-EEG, offering promising results for non-invasive characterization of the hemispheric functional organization of language in drug-resistant epileptic patients.