Mounting evidence in the past two decades has shown that the cognitively demanding experience of bilingualism affects brain structure1. Given that the majority of the world's population is bilingual2, bilingualism-induced neuroplasticity constitutes an appealing candidate for investigating how long-lasting demanding cognitive skills and experiences affect brain morphology3. However, using knowledge about bilingualism-induced neuroplasticity to draw conclusions about experience-dependent brain adaptations has been hampered by inconsistent results from studies in the field. Namely, existing research often reports structural changes in different regions and effects in different directions, including both volumetric increases and decreases4. While the field of bilingualism-induced neuroplasticity has generally embraced the basic assumption that demanding experiences can lead to neural adaptations, it has not examined the inconsistencies through the prism of general principles of experience-dependent neuroplasticity. In fact, experience-induced structural brain changes are often not linear, but rather dynamic, and they depend on the quality, quantity, and time course of experiences that trigger them5,6. Consequently, the exact dynamic nature of the effects of bilingualism on the brain might have remained overlooked. To address this issue, bilingualism needs to be approached as a continuous cognitively demanding experience, which can trigger dynamic structural adaptations.
The general brain mechanisms behind the acquisition of a new skill, such as learning a new language, resemble an audition 7. When facing a new cognitive challenge which cannot be met by the existing neural resources, brain expands to explore new candidates for efficient neural circuits to perform the newly emerged task. Upon selection of the most promising neural circuit resulting in required performance efficiency, the brain eliminates the superfluous neural resources. With respect to volumetric brain changes, the prominent theories argue for expansion-renormalisation model 5,7,8. According to it, initial volumetric increases related to skill acquisition are followed by decreases once the skill has been acquired and exercised efficiently. From this follows that cognitively demanding experiences often trigger brain adaptations that are not linear, but rather following an expansion-renormalisation trajectory.
Experience-depended neural adaptations are typically observed in brain regions which functionally support managing of the task at hand 9. In the case of second language learning (L2) and bilingual language use the critical regions are those subserving switching, cognitive and articulatory control, and language selection. Perhaps the most important of these regions are the basal ganglia (including structures such as caudate, putamen, globus pallidus and accumbens) and the thalamus 10,11. In general, these structures subserve integration of information from multiple cortical areas to select purposeful action in response to external stimuli or internal cues 12. It has been shown that language switching and selection of appropriate language systems allowing bilinguals to achieve fluent communication draws upon the cognitive-general functionality of basal ganglia and thalamus 10. Specifically, several studies reported recruitment of bilateral caudate during language-switching, and vocabulary learning 13–16. The globus pallidus and putamen have both been reported to engage in phonological monitoring and selection 17, while the putamen has also been implicated in the employment of motoric control schemata linked to language-specific articulatory demands 18. Activation of the nucleus accumbens has been explained by its role in maintaining the motivation to learn the second language 19. The thalamus, a region extensively connected with basal ganglia, has been implicated in language selection and, together with the globus pallidus, it subserves the coordination of motor routines related to language-specific articulatory motor programmes 20–22.
Evidence from structural studies confirms that the basal ganglia and the thalamus adapt structurally following bilingual practices. However, existing studies presented seemingly scattered patterns of these adaptations, often reporting effects in different regions, in different directions, or even absence of some effects altogether 1. For example, compared to monolinguals, bilinguals have generally been reported the have larger caudate nuclei, putamen, globus pallidus, and thalamus 23–25 but these effects tend to disappear in bilinguals immersed in bilingual context 26. Perhaps more confusingly, smaller caudate volumes have been reported in long-standing interpreters, that is exceptional bilinguals using both languages professionally, when compared to individuals with less cumulative interpreting experiences 27. These contrasting patterns have posed a challenge to the field in understanding the mechanisms that lead to bilingualism-induced adaptations.
Recall that a lot of this variability may be because of lack of understanding or systematic study of the dynamic nature of these adaptations. With respect to bilingualism, the Dynamic Restructuring Model (DRM) 4 builds on the expansion-renormalisation model 6 to conceptualise the bilingualism-induced brain changes. The DRM argues that in the case of bilingualism, structural brain adaptations are triggered by environmental changes in language control demands, which are determined by practices in bilingual language use and the amount of bilingual experiences. As such, the DRM offers a unifying theory explaining the divergent findings on brain changes brought about by bilingualism mentioned earlier.
We now turn to the specific predictions by the DRM on the regions of interest of the present paper, namely the basal ganglia and the thalamus. Individuals who start to learn a vocabulary of the second language face a new need to control between lexical alternatives for the same concepts. This assumedly triggers volumetric expansion of the caudate which subserves acquisition of new words in the second language 16 and lexical selection and control 10. Once bilinguals become proficient in both languages and start to engage with both languages more often, the most efficient networks get selected among the newly built neural resources. In turn, the volumetric expansion of caudate will reverse over time. This explains the variability in results in the studies mentioned above; volumes of caudate increase in less experienced bilinguals when compared to monolinguals, but these effects are absent in highly proficient bilinguals 26. Highly proficient bilinguals face new cognitive challenges linked to increased language production and control, which poses greater demands on language monitoring and motor control related to articulation. This explains the findings of increases in regions implicated in articulatory control and phonological selection in more experienced bilinguals, such as the left putamen 23,25 and globus pallidus 24. Similarly, more experienced bilinguals have a likely richer vocabulary, which leads to the growing need for lexical selection during production. This can explain the expansion of thalamic volumes, which is assumed to enable a more efficient selection mechanism 20.
In light of the above, acquisition and use of two or more languages resembles other complex skills in that it requires lifelong reconfiguration of the behavioural repertoire to address the altering cognitive demands. The DRM posits that such a longstanding dynamic process such as bilingualism brings about dynamic, non-linear effects on brain structure and that specific bilingual experiences can predict these effects. These experiences have been suggested to include onset of the second language (L2) acquisition 28, proportional usage of first (L1) and L2 29, duration of L2 use 30, L2 proficiency 31, linguistic differences between L1 and L2 32, and intensity of switching between the languages 33. Nevertheless, the DRM predictions remain formulated based on the synthesis of results from single studies which largely used between-groups comparisons (e.g. bilinguals vs. monolinguals). Such an approach cannot account for the variability in the aforementioned individual bilingual experiences. Instead, treating bilingualism as a continuous rather than categorical variable and looking at the variability withing a bilingual sample has been called upon as an alternative approach with a potential to contribute new insights in the effects of bilingualism on the mind and brain 34,35.
Following from these suggestions, a recent study applied an experienced-based approach in revealing dynamic changes of neural adaptations in bilinguals 19. To quantify bilingual experiences, the Language and Social Background Questionnaire (LSBQ)36 was used, which provides continuous measures of bilingual use in different contexts. The study revealed expansions of left accumbens, caudate and right thalamus to be predicted by social language use, whereas age of language acquisition predicted both expansions and contractions in parts of right caudate and putamen and contractions in bilateral accumbens and thalamus. These results support the notion that bilingual experiences assessed on a continuum can reveal complex patterns of brain adaptations. Critically however, these analyses assumed linear structural adaptations. Treating effects of bilingualism linearly disallows for testing of predictions rooted in evidence that demanding experiences can have non-linear effects on brain structure. Therefore, it is crucial to allow for non-linearity of these effects in order to examine the evidence-based DRM predictions that changes brought about by bilingualism are dynamic.
In point of fact, prominent theories of experience-dependent neuroplasticity advocate against assuming linear brain volume growth during skill acquisition (for review, see Wenger et al., 2017), with some even calling assumed continual increase in brain volumes unfeasible 37. With respect to bilingualism, Pliatsikas and colleagues (2021) used Generalised Additive Mixed Models (GAMMs), a statistical method that can reveal non-linear effects, to study concentrations of brain metabolites in the basal ganglia as a function of bilingual experiences. Among other markers, they investigated concentrations of myo-Inositol (INS) and N-acetyl aspartate (NAA), which have been treated as markers of the processes that underlie neuroplasticity, such as synaptic pruning and repurposing of neural substrates. They revealed that bilingual experiences predicted these concentrations in a non-linear fashion. The authors interpreted this as indirect evidence for microscopic experience-based restructuring of the basal ganglia, signifying increases in synaptic connections and also the elimination of the superfluous synapses depending on the amount of bilingual experiences. Such an interpretation is in accordance with the DRM. However, it remains to be determined whether such non-linear adaptations observed on the microscopic level occur also at the level of volumes of relevant brain structures.
Following up from this approach, in the present study we employ GAMMs to model non-linear effects of continuous measures of bilingual experiences on volumes of basal ganglia and thalamus across a rich sample of bilinguals with a wide range of bilingual experiences. Specifically, our sample ranges from bilinguals with limited opportunity for active bilingual languages use, to advanced bilinguals and translators, who engage with two languages daily, to exceptional bilinguals such as interpreters, who face extreme control demands in their jobs. The dynamicity of bilingualism is captured on the continuum using the LSBQ composite score (henceforth Bilingual composite score; BCS), which spans information about language proficiency, exposure, switching, and duration and proportionality of the use of both languages36.
Based on DRM, we predicted distinct trajectories of volumetric adaptations of basal ganglia and thalamus as a function of quantified bilingual experiences. Specifically, we expected an expansion-renormalisation pattern of the caudate, expressed as a trajectory suggesting increases in volume with limited bilingual experience, which will however plateau and eventually decrease as bilingual experience increases. A similar pattern was also predicted for the neighbouring nucleus accumbens, a region that is strongly interconnected with the caudate nucleus and has also been shown to contract in experienced bilinguals 19. According to the DRM, adaptations of putamen and globus pallidus have been suggested to come after the onset of caudal changes. With respect to the putamen, we expect to observe a pattern consistent with onset of structural brain adaptations in bilinguals with larger amount of bilingual experiences than for the caudate and the accumbens. If putamen will manifest renormalisation, we predict that this will occur only in individuals at the highest end of the spectrum of bilingual experiences. Globus pallidus has received less attention than the neighbouring putamen. However, we expect comparable patterns as in putamen due to the interrelatedness of both structures, and their shared functionality 26. Expansions of thalamus have been reported in long-standing, regularly practicing bilinguals whose brain has reached efficiency in the mechanisms that undertake vocabulary learning and control 19. It has been suggested to be involved together with globus pallidus in coordinating of motor programmes 39, a function employed for successful articulation of different languages. Taken together, we expect to observe comparable adaptation patterns as in putamen and globus pallidus, i.e., later onset of thalamic volumes increases relative to caudate with possible renormalisation only in bilinguals with high level of bilingual experiences.