The influence of bilingualism on gray matter volume in the course of aging: a longitudinal study

Abstract

Background: Bilingualism is associated with higher gray matter volume (GMV) as a form of brain reserve in brain regions such as the inferior frontal gyrus (IFG) and the inferior parietal lobule (IPL). A recent cross-sectional study reported the age-related GMV decline in the left IFG and IPL to be steeper for bilinguals than for monolinguals. The present study aimed at supporting this finding for the first time with longitudinal data.

Methods: In the current study, 200 participants aged 19 to 79 years (87 monolinguals, 113 sequential bilinguals, mostly native German speakers with variable second language background) were included. Trajectories of GMV decline in the bilateral IFG and IPL were analyzed in mono- and bilinguals over two time points (mean time interval: 3.6 years). For four regions of interest (left/right IFG and left/right IPL), mixed Analyses of Covariance were conducted to assess (i) GMV changes over time, (ii) GMV differences for language groups (monolinguals/bilinguals), and (iii) the interaction between time point and language group. Corresponding analyses were conducted for the two factors of GMV, surface area (SA) and cortical thickness (CT).

Results: There was higher GMV in bilinguals compared to monolinguals in the IPL, but not IFG. While the left and right IFG and the right IPL displayed a similar GMV change in mono- and bilinguals, GMV decline within the left IPL was significantly steeper in bilinguals. There was greater SA in bilinguals in the bilateral IPL and a steeper CT decline in bilinguals within in the left IPL.

Conclusion: The cross-sectional observations of a steeper GMV decline in bilinguals could be confirmed for the left IPL. Additionally, the higher GMV in bilinguals in the bilateral IPL may indicate that bilingualism contributes to brain reserve especially in posterior brain regions. SA appeared to contribute to bilinguals' higher GMV in the bilateral IPL, while CT seemed to account for the steeper structural decline in bilinguals in the left IPL. The present findings demonstrate the importance of time as an additional factor when assessing the neuroprotective effects of bilingualism on structural features of the human brain.

Keywords: aging; bilingualism; brain reserve; gray matter volume; inferior frontal gyrus; inferior parietal lobule.

FIGURE 1

The inferior frontal gyrus (IFG) and the inferior parietal lobule (IPL) in the left (A) and right (B) hemisphere based on the cytoarchitectonic probabilistic Jülich-Brain atlas (Amunts et al., 2020).

FIGURE 2

GMV change over time separately for each participant of the present study for the left (A) and right IFG (B) as well as for the left (C) and right IPL (D). The gray underlay indicates participants ≥ 55 years at time point t1, who were included in the subsample. GMV, gray matter volume; IFG, inferior frontal gyrus; IPL, inferior parietal lobule.

FIGURE 3

GMV change over time in mono- and bilinguals in the left IPL. For both language groups, mean GMV and standard error of the mean are depicted for t1 and t2 as well as ΔV, i.e., the mean absolute GMV difference between t1 and t2. The GMV decline over time is significantly steeper in bilinguals. GMV, gray matter volume; IPL, inferior parietal lobule; t1, first time point; t2, second time point.

FIGURE 4

Two models of GMV change over the course of time in mono- and bilinguals. While GMV change in monolinguals is sketched as continuous GMV decline, three stages of dynamic structural change are depicted for bilinguals, as suggested in the “dynamic restructuring model” (DRM; Pliatsikas, 2020): Learning an additional language results in increasing GMV, followed by GMV decrease during the phase of consolidation. With aging, the decline in left-hemispheric language areas is steeper in bilinguals than in monolinguals (A). Hence, the volume differences between monolinguals and bilinguals disappear over time, possibly reflecting an ongoing selection of most efficient neural circuits in bilinguals with continuous bilingual experience. Thus, bilingualism might result in constantly increasing efficiency with regards to language processing. In right-hemispheric regions related to domain-general control, the decrease in bilinguals attenuates until it matches monolingual decline (B). Thus, bilingualism may provide a persistent brain reserve in the non-linguistic domain. Figures adapted from Heim et al. (2019).

FIGURE 5

A model of shifts in task-induced neural activity in mono- and bilinguals in the course of aging (dashed lines) and bilingualism (solid lines). With aging, a “posterior-to-anterior-shift” (PASA; Davis et al., 2008) and a “hemispheric asymmetry reduction” (HAROLD; Cabeza, 2002) can be observed (in terms of language, which is usually processed in the left hemisphere, HAROLD predicts an increased recruitment of the right hemisphere with aging, as depicted here). In monolinguals, this leads to increasing prefrontal activation with aging (A). In bilinguals, however, an “anterior-to-posterior and subcortical shift” (BAPSS; Grundy et al., 2017) occurs with increasing bilingual experience, which may counteract age-related changes predicted by PASA (B). Therefore, BAPSS may represent a form of cognitive reserve in bilinguals. Additionally, the interaction of BAPSS and HAROLD may lead to increasing use of the right IPL with aging in bilinguals, but not monolinguals, possibly resulting in an attenuation of structural decline in bilinguals in the right IPL.