Can bilingualism increase neuroplasticity of language networks in epilepsy?

Abstract

Individuals with left temporal lobe epilepsy (TLE) have a higher rate of atypical (i.e., bilateral or right hemisphere) language lateralization compared to healthy controls. In addition, bilinguals have been observed to have a less left-lateralized pattern of language representation. We examined the combined influence of bilingual language experience and side of seizure focus on language lateralization profiles in TLE to determine whether bilingualism promotes re-organization of language networks. Seventy-two monolingual speakers of English (21 left TLE; LTLE, 22 right TLE; RTLE, 29 age-matched healthy controls; HC) and 24 English-dominant bilinguals (6 LTLE, 7 RTLE, 11 HC) completed a lexical-semantic functional MRI task and standardized measures of language in English. Language lateralization was determined using laterality indices based on activations in left vs right homologous perisylvian regions-of-interest (ROIs). In a fronto-temporal ROI, LTLE showed the expected pattern of weaker left language lateralization relative to HC, and monolinguals showed a trend of weaker left language lateralization relative to bilinguals. Importantly, these effects were qualified by a significant group by language status interaction, revealing that bilinguals with LTLE had greater rightward language lateralization relative to monolingual LTLE, with a large effect size particularly in the lateral temporal region. Rightward language lateralization was associated with better language scores in bilingual LTLE. These preliminary findings suggest a combined effect of bilingual language experience and a left hemisphere neurologic insult, which may together increase the likelihood of language re-organization to the right hemisphere. Our data underscore the need to consider bilingualism as an important factor contributing to language laterality in patients with TLE. Bilingualism may be neuroprotective pre-surgically and may mitigate post-surgical language decline following left anterior temporal lobectomy, which will be important to test in larger samples.

Keywords: Bilingualism; Functional magnetic resonance imaging (fMRI); Language lateralization; Laterality; Neuroplasticity; Temporal lobe epilepsy.

Figure 1.. Selected regions of interest.

Two language regions of interest (ROIs) selected for fMRI analysis using the Destrieux atlas. The inferior frontal region consists of the opercular, orbital, and triangular parts of the inferior frontal gyrus and the inferior frontal sulcus. The lateral temporal region consists of the middle temporal gyrus, superior temporal gyrus, and the superior temporal sulcus. These two regions were combined to produce an omnibus language LI which was used as the main outcome variable in analyses.

Figure 2.. Individual and whole-brain statistical maps for the contrast of interest (novel words minus false fonts) that isolates lexical-semantic processing.

Whole-brain statistical t-maps are shown for: A) monolingual healthy controls (HC), B) bilingual HC, C) monolingual left TLE (LTLE), D) bilingual LTLE and E) single-subject maps for each B-LTLE participant that corresponds to a case number in Table 2. Monolingual group maps and B-LTLE individual subject maps were cluster-corrected at p < .05 with a voxel-wise correction of p < .01. We used a more liberal threshold for the two bilingual group maps for purposes of visualization and due to smaller sample size (<20 per group), using a cluster-correction of p < .05 and voxel-wise p < .10. Group maps for RTLE looked similar to controls and are presented in Supplementary Figure 1. Of note, all reported statistical analyses were carried out using ROIs in native space with a stringent correction (see Methods).

Figure 3.. The effect of group on language lateralization is dependent on language status.

fMRI laterality index (LI) plotted separately by group (age-matched controls; HC, left TLE; LTLE, and right TLE; RTLE) and language status (bilingual, monolingual) for A) omnibus language LI, B) inferior frontal LI, and C) lateral temporal LI. Right- and left-handed/ambidextrous individuals are coded as circles and triangles, respectively. Yellow diamonds represent group means. Individuals below the horizontal dotted line have atypical language lateralization (LI ≤ 0.2). Rates of atypical (i.e., right or bilateral) lateralization based on omnibus LI were as follows: monolingual HC=7% (2/29), bilingual HC=0% (0/11), monolingual LTLE=14% (3/21), bilingual LTLE (67%; 4/6), monolingual RTLE=18% (4/22) and bilingual RTLE=0% (0/7). Boxplot denotes the median (bold bar), first and third quartiles (box limits), and ±1.5 times the interquartile range (whiskers).

Figure 4.

Panels A-C plot raw scores on standardized language measures by group (left TLE; LTLE, right TLE; RTLE, healthy controls; HC) and language status (bilingual, monolingual) separately for A) category fluency, B) letter fluency, and C) auditory naming.

Figure 5.. The relationship between language lateralization and language function.

Language z-scores as a function of laterality indices (LIs) derived from fMRI (x-axis), plotted separately for bilingual LTLE (B-LTLE; red circles) and monolingual LTLE (M-LTLE; green triangles). Panels A-C depict lateral temporal LI, panels D-F depict inferior frontal LI, and panels G-I depict the omnibus language LI by each language measure (category fluency, letter fluency, and auditory naming). X-axis values to the left of the dashed vertical black line represent atypical language lateralization, and y-axis values below the dashed horizontal black line represent impaired language scores.