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Bilingualism
Bilingualism J Abutalebi and D Perani, University San Raffaele, Milan, Italy ã 2015 Elsevier Inc. All rights reserved.
Introduction The human brain not only has evolved to accommodate a single language but also is, in fact, suited to acquire more than one language, such as the case of bilingual and multilingual individuals. As globalization advances, more people become bilingual or multilingual thus establishing bilingualism as the standard rather than the exception (Grosjean & Li, 2013). A bilingual individual may achieve different levels of proficiency in the two languages, using both languages in different contexts, by learning a new language following educational requirements, immigration, or alternative circumstances. By this definition, a bilingual individual is not only necessarily someone who has acquired both languages from birth, or early in life, but also that one who learns a second language (L2) later in life. The different contexts and circumstances of L2 acquisition have important effects upon the cerebral organization of multiple languages. Moreover, having acquired more than one language, the bilingual or multilingual speaker may eventually encounter potential conflicts between said languages, such as how to speak in one language while avoiding potential intrusions from the other. As a broad definition, the concept of neural representation of bilingualism refers to functional and structural neuroimaging evidence that provided the cerebral organization of two (or more) languages. These studies focus on not only how two or more languages are anatomically represented in the human brain, according to crucial variables such as proficiency, age of acquisition (AOA), and exposure, but also, ultimately, how individuals acquire, process, and eventually may later lose such languages. From a historical viewpoint, the landmark study of Pitres (1895) marked the initiation of this field and has enticed the interest of researchers for more than a century. Pitres in 1896 described cases of selective loss and recovery of a given language in bilingual aphasics, thus giving rise to vivid discussions about different potential neural locations for languages. Indeed, prior to the advent of functional neuroimaging, it was widely believed that bilingual language representation was assigned to different brain areas or even different hemispheres (Albert & Obler, 1978). This hypothesis was essentially based on the common observation of bilingual aphasics who recover only one language after stroke, while the other is lost; this led researchers to believe that the brain regions responsible for one language was damaged though the others remained intact. However, functional neuroimaging studies have so far contradicted this assumption (see, for review, Abutalebi, 2008; Indefrey, 2006; Perani & Abutalebi, 2005). Today, it is well established that bilinguals use the same neural substrate, thus identical brain structures for both languages. The neural networks can vary according to variables that influence neural plasticity, among those, the exposure or amount of use to a given language.
Brain Mapping: An Encyclopedic Reference
In this article, we will provide a brief overview of how two or more languages are organized in the human brain and what mediates their processes.
The Neural Representation of L2 For successful acquisition of an L2, an entire new set of phonological, lexico-semantic, and morphosyntactic knowledge, which is largely distinctive from the first language (L1), needs to be mentally stored and instantiated. In the case of L1 acquisition, the shaping and organization of such linguistic knowledge usually lead to a fairly effortless tuning of all cognitive processes subtending language. The same phenomenon manifests when an L2 is learned from birth or very early in life (i.e., before age 6) (Wartenburger et al., 2003). However, this rarely occurs for an L2 learned after early childhood. A crucial question to unravel is whether L2 learning is constrained by the ‘critical time period’ that is paralleled in neural terms with maturational changes in the brain (McDonald, 2000). According an influential account, that is, the critical period hypothesis (CPH) (Birdsong, 2006; Johnson & Newport, 1989), there is a critical period in acquiring full competence (phonological, lexico-semantic, and morphosyntactic representations) in two (or more) languages. On this basis, researchers have hypothesized a fundamental difference between L1 acquisition and L2 learning.
Neural Representation of L2 Grammar The aforementioned CPH hypothesizes the existence of a purported critical period for acquisition of phonology, morphology, and syntax (Birdsong, 2006; Johnson & Newport, 1989). In the case of morphology and syntax, the declarative/procedural model (DP) (Ullman, 2001) attempted to provide a rationale for putative differences. DP claims that in normal monolinguals, words are represented in a declarative (i.e., explicit) memory system, whereas grammatical rules are represented through a cognitive system that mediates the use of procedural memory (i.e., implicit memory processed without conscious awareness). Following the DP model, when an L2 is learned after the critical period, it can no longer rely on the procedural/implicit resources that are used for L1 grammatical processes. Rather, grammatical knowledge in L2 would be processed using explicit resources (much like L1 and L2 words). Furthermore, since procedural knowledge and declarative knowledge are mediated by distinct neural systems (i.e., Broca’s area and the basal ganglia and left temporal areas, respectively), late L2 learners would rely more heavily on posterior brain areas, (left temporal areas responsible for lexicosemantic processing and hence declarative knowledge) when
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compared with L1 speakers (Broca’s area and the basal ganglia), when computing L2 grammar (Ullman, 2001). It is worth emphasizing that functional neuroimaging studies have, so far, contradicted this assumption (see for review Abutalebi, 2008). Crucially, Sakai, Miura, Narafu, and Muraishi (2004) reported that the acquisition of grammatical competences in late bilingual twins is achieved through the same neural structures used in processing L1 grammar, that is, Broca’s area. Likewise, in an fMRI study investigating L2 verb conjugation (Sakai et al., 2004) and past tense word processing (Tatsuno & Sakai, 2005), increased activity in the areas mediating L1 syntax (i.e., Broca’s area) was reported, but not in posterior brain areas, as postulated by the DP model. Additional evidence was reported in studies investigating artificial grammar learning (Friederici, Bahlmann, Helm, Schubotz, & Anwander, 2006; Opitz & Friederici, 2004); acquisition of language-like rules of an artificial language was associated with increased recruitment of Broca’s area. These results support the notion that learning L2 grammar (albeit an artificial one) is carried out through the preexisting neural network that mediates native language grammar. As to the precise network mediating syntax in monolinguals, Friederici (2011) reported that syntactical processes are carried out by the frontal operculum (FOp) along with the anterior part of the superior temporal gyrus (STG). This network is responsible for both natural grammar processing in monolinguals and artificial grammar processing. However, as Friederici (2011) underlined, under less proficient processing conditions such as language learning in developmental ages or L2 learning, the network comprises not only the FOp an STG but also Broca’s area and surrounding areas and potentially also the basal ganglia. L2 grammar learning usually arises in the context of an already-specified language system (i.e., L1). Since the neural system underlying grammatical processes, including Broca’s area, has learned to compute grammatical processing for the native language (L1) during the developmental stages, it is likely that the same kind of neural computation is valid also for an eventual L2. Differences may arise in the initial stages of L2 learning, where a need of additional brain substrate for processing the newly learned L2 is required; but these neural differences seem to vanish once the proficiency becomes comparable to that of L1 (Consonni et al., 2013). In this specific case, the neural representation of L2 converges to that of L1, as suggested by Green (2003). As shown by functional neuroimaging, there is more brain activity for an L2 (especially when processed with a nonnative-like proficiency) in Broca’s area and surrounding regions. Following Indefrey (2006), bilinguals might compensate for lower efficiency in L2 by involving these regions more strongly.
Neural Representation of L2 Phonology Similar to grammar processing, critical periods have been postulated for phonological processing (Singleton, 2005). Correctly perceiving and producing the foreign language sounds are challenging tasks. Problems of this kind are reported even for individuals who have been exposed for considerable periods of time to an L2 (Pallier, Bosch, & SebastianGalle´s, 1997).
From a neuroanatomical perspective, phonetic perception and production appear to be carried out through specialized networks in the left hemisphere, such as Wernicke’s area, the left inferior parietal lobe, and Broca’s area, as shown by functional neuroimaging (De´monet, Thierry, & Cardebat, 2005). Again, one may pose the question as to whether L2 phonological representations are acquired, stored, and processed in a different fashion from that of the native language. Again, neuroimaging studies consistently provide evidence for a shared neural network for L1 and L2 phoneme perception and production (e.g., Heim & Friederici, 2003). Although the functional neuroimaging literature on phonological processing in bilinguals is rather limited (as compared to the many studies investigating morphosyntactic and lexico-semantic processing), some conclusions may be drawn: the available evidence shows that L2 phonology is essentially acquired and processed through the same neural structures mediating L1 phonology, that is, a network comprising the FOp, the supramarginal gyrus, and the left putamen. Some neuroimaging studies showed an increased extension of brain activity, indicating that overall L2 processing requires greater recruitment of neural resources. One reason for this observation might be that these studies have included late and low-proficiency L2 learners (i.e., Callan, Jones, Callan, & Yamada, 2004; Callan et al., 2003; Wang, Xue, Chen, Xue, & Dong, 2007) or monolingual subjects who, for the experimental purpose, were asked to learn phonetic contrasts in a foreign language (Golestani & Zatorre, 2004). In the latter case, it is possible that the greater brain activity may reflect the accommodation of a new set of sounds by the existing native speech system rather than the acquisition of a nonnative phonetic contrast in an L2 context. In the former case (i.e., L2 English speakers), it is plausible that processing sounds in L2, subserved by less calibrated representations, may require greater cognitive effort and therefore greater neuronal activity than processing sounds in L1.
Neural Representation of L2 Lexico-Semantics In the context of the lexico-semantic domain, the most influential cognitive model, that is, the revised hierarchical (RH) model (Kroll & Stewart, 1994), claims that separate lexical memory systems contain words for each of the two languages, whereas semantic concepts are stored in an abstract memory system common to both languages. Following this account, at the beginning stage of L2 acquisition, L2–L1 mediation would mainly occur between direct translations at the lexical level (i.e., L2 words are mentally translated into L1 words). However, with increasing L2 proficiency, L2 words would become more tightly bound to their specific conceptual representations and would be less dependent upon their L1 translation equivalent. Notably, following the RH model, lexical processing would be independent of the AOA of L2 and critical periods but would rather rely mostly on language proficiency. This is in line with Green’s convergence theory (2003) that postulates that many of the qualitative differences between native and L2 speakers disappear as proficiency increases. Regarding the neuroanatomical basis of the lexico-semantic system in bilinguals, functional neuroimaging studies, at the single word level, such as picture naming, verbal fluency, word completion, and word repetition tasks, have been consistently
INTRODUCTION TO COGNITIVE NEUROSCIENCE | Bilingualism
reported that L1 and L2 entail common neural activations in the left frontal and temporoparietal brain areas. This is true when the degree of L2 proficiency is comparable to L1 (Abutalebi, 2008). There are exceptions for bilinguals with different alphabetic scripts and bimodal bilinguals (see the succeeding text). Notably, these networks are identical to those commonly engaged when monolinguals perform the same kind of language tasks. On the other hand, bilinguals with low proficiency and/or low exposure to L2 engaged additional brain activity (Perani et al., 2003). At the single word level, the pattern of brain activation for L1 and L2 seems to converge; however, brain activation for more complex comprehension processes, such as sentencelevel comprehension, shows differences associated with the eventual workload of the task. Differences in brain activation between L1 and L2 have been found as more extended activations in prefrontal regions with increased cognitive workload in a listening comprehension task (Hasegawa, Carpenter, & Just, 2002) and in a frontal–parietal network related to phonological processes in a reading comprehension task (Buchweitz, Mason, Hasegawa, & Just, 2009). Studies also showed recruitment of additional brain networks to accommodate the processing demands of different writing conventions (different writing systems and scripts such as English and Chinese) (Perfetti et al., 2007; Tan et al., 2001). Hence, the level of dynamic distribution of brain activity in L2 compared with L1 is accounted for not only the differences in degrees of L2 proficiency but also the workload and eventually the linguistic distance. Interestingly, in addition to different activation associated with proficiency, workload, and orthographic systems, it is important to underline that the investigation of bimodal bilinguals (signed and spoken languages) may further widen our knowledge into converging processes across languages: in the
special case of bimodal bilinguals, processes associated with different languages conveyed in different modalities. A recent study showed that despite large similarities in the brain activation associated with spoken and sign-language production, bimodal bilinguals, in comparison with monolinguals, showed more right-hemisphere temporal and occipital activation during a sign-language task. The additional righthemisphere areas recruited may support cognitive processes specifically associated with sign-language production (Zou, Ding, Abutalebi, Shu, & Peng, 2012; Zou, Abutalebi, et al., 2012).
Language Control and Neural Consequences Induced by Bilingualism Common to the aforementioned studies are the findings of additional brain activity during L2 processing as compared with L1 processing. This extra activity is usually reported when the level of proficiency of L2 is not native-like, or when the task load is different, or crucially when the amount of exposure to a given language varies. Indeed, recent studies have shown that even in early and high-proficiency bilinguals, the amount of exposure and usage of languages does result in differential activity (Abutalebi et al., 2007; Perani et al., 2003). As to the precise location of the extra activity, it is found mostly in the prefrontal areas (Abutalebi, 2008) and eventually also in the anterior cingulate cortex (ACC), the left inferior parietal lobule, and the left caudate (see Figure 1). Interestingly, this set of brain areas is usually linked to executive control and not specifically to language processing. Findings indicating that low-proficiency bilinguals rely on executive control areas when processing a weak L2 may suggest that they are in need of greater mental coordination in order to
preSMA /ACC
Pre frontal
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Figure 1 The language control network in bilinguals. Adapted from Abutalebi, J., & Green, D. (2007). Bilingual language production: The neurocognition of language representation and control. Journal of Neurolinguistics, 20, 242–275.
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speak an L2 unerringly. Abutalebi and Green (2007) referred to this processes as language control. Language control more precisely refers to the unique ability of bilinguals to suppress one language while speaking the other. This ability is strictly necessary for preventing that items of the language not in use slip into the language in use. However, the need to control and monitor the two languages may also induce a cost by increasing the effort bilinguals need to make especially in speech production tasks (Abutalebi & Green, 2007; Kroll, Bobb, Misra, & Guo, 2008). Consistent with this view, several investigations have shown a greater engagement of brain areas implicated in language control in bilinguals as compared with monolinguals. For example, Abutalebi and collaborators have convincingly argued that the head of the left caudate and the left ACC are especially recruited during bilingual language processing (Abutalebi et al., 2008; Abutalebi, Della Rosa, Ding, et al., 2013; Garbin et al., 2011), suggesting that such structures are crucially involved in keeping the two languages apart during language processing, at least in contexts in which both languages are engaged (see Zou, Ding, et al., 2012 for similar evidence with bimodal bilinguals). A very interesting recent discovery in this context is the fact that bilingualism induces also structural changes in the brain. Bilingualism induces experience-related structural changes (i.e., in terms of increased gray or white matter density) in the frontal lobes (Luk, Bialystok, Craik, & Grady, 2011), the left inferior parietal lobule (Della Rosa et al., 2013; Mechelli et al., 2004), the ACC (Abutalebi et al., 2012), and subcortical structures such as the left caudate (Zou, Ding, et al., 2012) and left putamen (Abutalebi, Della Rosa, Castro Gonzaga, et al., 2013). These areas are part of the executive control network and the reason why bilinguals usually have a cognitive advantage in executive control tasks over monolinguals; that is, bilinguals are faster to resolve cognitive conflicts than monolinguals (Bialystok, Craik, & Luk, 2012). Noteworthy, a relevant direct consequence of these structural changes in the executive control network is the promotion of cognitive reserve in elderly people: elderly bilinguals outperform monolinguals in executive control tasks and appear to have a 4–5-year onset delay of behavioral symptoms associated to neurodegenerative diseases such dementia as compared with monolinguals (Alladi et al., 2013; Bialystok et al., 2012).
See also: INTRODUCTION TO ANATOMY AND PHYSIOLOGY: Lateral and Dorsomedial Prefrontal Cortex and the Control of Cognition; INTRODUCTION TO CLINICAL BRAIN MAPPING: Disorders of Language; INTRODUCTION TO COGNITIVE NEUROSCIENCE: The Neurobiology of Sign Language; INTRODUCTION TO SYSTEMS: Grammar and Syntax.
References Abutalebi, J. (2008). Neural processing of second language representation and control. Acta Psychologica, 128, 466–478. Abutalebi, J., Annoni, J. M., Seghier, M., Zimine, I., Lee-Jahnke, H., Lazeyras, F., et al. (2008). Language control and lexical competition in bilinguals: An event-related fMRI study. Cerebral Cortex, 18, 1496–1505. Abutalebi, J., Brambati, S. M., Annoni, J. M., Moro, A., Cappa, S. F., & Perani, D. (2007). The neural cost of the auditory perception of language switches: An eventrelated fMRI study in bilinguals. Journal of Neuroscience, 27, 13762–13769.
Abutalebi, J., Della Rosa, P. A., Castro Gonzaga, A., Keim, R., Costa, A., & Perani, D. (2013). The role of the left putamen in multilingual language production. Brain and Language, 125, 307–315. Abutalebi, J., Della Rosa, P. A., Ding, G., Weekes, B. S., Costa, A., & Green, D. W. (2013). Language proficiency modulates the engagement of cognitive control areas in multilinguals. Cortex, 49, 905–911. Abutalebi, J., Della Rosa, P. A., Green, D. W., Hernandez, M., Scifo, P., Keim, R., et al. (2012). Bilingualism tunes the anterior cingulate cortex for conflict monitoring. Cerebral Cortex, 22, 2076–2086. Abutalebi, J., & Green, D. (2007). Bilingual language production: The neurocognition of language representation and control. Journal of Neurolinguistics, 20, 242–275. Albert, M. L., & Obler, L. K. (1978). The bilingual brain. New York: Academic Press. Alladi, S., Bak, T. H., Duggirala, V., Surampudi, B., Shailaja, M., Kumar Shukla, A., et al. (2013). Bilingualism delays age at onset of dementia, independent of education and immigration status. Neurology, 81, 1938–1944. Bialystok, E., Craik, F. I., & Luk, G. (2012). Bilingualism: Consequences for mind and brain. Trends in Cognitive Sciences, 16, 240–250. Birdsong, D. (2006). Age and second language acquisition and processing: A selective overview. Language Learning, 56, 9–49. Buchweitz, A., Mason, R. A., Hasegawa, M., & Just, M. A. (2009). Japanese and English sentence reading comprehension and writing systems: An fMRI study of first and second language effects on brain activation. Bilingualism: Language and Cognition, 12, 141–151. Callan, D. E., Jones, J. A., Callan, A. K., & Yamada, R. A. (2004). Phonetic perceptual identification by native- and second-language speakers differentially activates brain regions involved with acoustic phonetic processing and those involved with articulatory–auditory/orosensory internal models. NeuroImage, 22, 1182–1194. Callan, D. E., Tajima, K., Callan, A. M., Kubo, R., Masaki, S., & Akahane-Yamada, R. (2003). Learning-induced neural plasticity associated with improved identification performance after training of a difficult second language phonetic contrast. NeuroImage, 19, 113–124. Consonni, M., Cafiero, R., Marin, D., Tettamanti, M., Iadanza, A., Fabbro, F., et al. (2013). Neural convergence for language comprehension and grammatical class production in highly proficient bilinguals is independent of age of acquisition. Cortex, 49, 1252–1258. Della Rosa, P. A., Videsott, G., Borsa, V. M., Canini, M., Weekes, B., Franceschini, R., et al. (2013). A neural interactive landmark for multilingual talent. Cortex, 49, 605–608. De´monet, J. F., Thierry, G., & Cardebat, D. (2005). Renewal of the neurophysiology of language: Functional neuroimaging. Physiological Reviews, 85, 49–95. Friederici, A. D. (2011). The brain basis of language processing: From structure to function. Physiological Reviews, 91, 1357–1392. Friederici, A. D., Bahlmann, J., Helm, S., Schubotz, R. I., & Anwander, A. (2006). The brain differentiates human and non-human grammars: Functional localization and structural connectivity. Proceedings of the National Academy of Sciences of the United States of America, 103, 2458–2463. Garbin, G., Costa, A., Sanjuan, A., Forn, C., Rodriguez-Pujadas, A., Ventura, N., et al. (2011). Neural bases of language switching in high and early proficient bilinguals. Brain and Language, 119, 129–135. Golestani, N., & Zatorre, R. J. (2004). Learning new sounds of speech: Reallocation of neural substrates. NeuroImage, 21, 494–506. Green, D. W. (2003). The neural basis of the lexicon and the grammar in L2 acquisition. In R. van Hout, A. Hulk, F. Kuiken, & R. Towell (Eds.), The interface between syntax and the lexicon in second language acquisition. Amsterdam: John Benjamins. Grosjean, F., & Li, P. (2013). The psycholinguistics of bilingualism. New York: Wiley. Hasegawa, M., Carpenter, P., & Just, M. A. (2002). An fMRI study of bilingual sentence comprehension and workload. NeuroImage, 15, 647–660. Heim, S. T., & Friederici, A. D. (2003). Phonological processing in language production: Time course of brain activity. NeuroReport, 14, 2031–2033. Indefrey, P. (2006). A meta-analysis of hemodynamic studies on first and second language processing: Which suggested differences can we trust and what do they mean? Language Learning, 56, 279–304. Johnson, J. S., & Newport, E. L. (1989). Critical period effects in second language learning: The influence of maturational state on the acquisition of English as a second language. Cognitive Psychology, 21, 60–99. Kroll, J. F., Bobb, S. C., Misra, M., & Guo, T. (2008). Language selection in bilingual speech: Evidence for inhibitory processes. Acta Psychologica, 128, 416–430. Kroll, J. F., & Stewart, E. (1994). Category interference in translation and picture naming: Evidence for asymmetric connections between bilingual memory. Journal of Memory and Language, 33, 149–174. Luk, G., Bialystok, E., Craik, F., & Grady, C. (2011). Lifelong bilingualism maintains white matter integrity in older adults. Journal of Neuroscience, 31, 16808–16813.
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McDonald, J. (2000). Grammaticality judgments in a second language: Influences of age of acquisition and native language. Applied Psycholinguistics, 21, 395–423. Mechelli, A., Crinion, J. T., Noppeney, U., O’Doherty, J., Ashburner, J., Frackowiack, R. S., et al. (2004). Neurolinguistics: Structural plasticity in the bilingual brain. Nature, 431, 757. Opitz, B., & Friederici, A. D. (2004). Interactions of the hippocampal system and the prefrontal cortex in learning language-like rules. NeuroImage, 19, 1730–1737. Pallier, C., Bosch, L., & Sebastian-Galle´s, N. (1997). A limit on behavioral plasticity in speech perception. Cognition, 64, 9–17. Perani, D., & Abutalebi, J. (2005). Neural basis of first and second language processing. Current Opinion in Neurobiology, 15, 202–206. Perani, D., Abutalebi, J., Paulesu, E., Scifo, P., Cappa, S. F., & Fazio, F. (2003). The role of language dominance and usage in early high proficient bilinguals. Human Brain Mapping, 19, 170–182. Perfetti, C., Liu, Y., Fiez, J., Nelson, J., Bolger, D. J., & Tan, L.-H. (2007). Reading in two writing systems: Accommodation and assimilation of the brain’s reading network. Bilingualism: Language and Cognition, 10, 131. Pitres, A. (1895). Etude sur l’aphasie chez les polyglottes. Revue de me´decine, 15, 873–899. Sakai, K. L., Miura, K., Narafu, N., & Muraishi, Y. (2004). Correlated functional changes of the prefrontal cortex in twins induced by classroom education of second language. Cerebral Cortex, 14, 1233–1239.
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Singleton, D. (2005). The critical period hypothesis: A coat of many colours. International Review of Applied Linguistics in Language Teaching, 43, 269–285. Tan, L. H., Liu, H. L., Perfetti, C. A., Spinks, J. A., Fox, P. T., & Gao, J. H. (2001). The neural system underlying Chinese logograph reading. NeuroImage, 13, 836–846. Tatsuno, Y., & Sakai, K. L. (2005). Language related activations in the left prefrontal regions are differentially modulated by age, proficiency and task demands. Journal of Neuroscience, 16, 1637–1644. Ullman, M. T. (2001). A neurocognitive perspective on language: The declarative/ procedural model. Nature Reviews. Neuroscience, 2, 717–726. Wang, Y., Xue, G., Chen, C., Xue, F., & Dong, Q. (2007). Neural bases of asymmetric language switching in second-language learners: An ER-fMRI study. NeuroImage, 35, 862–870. Wartenburger, I., Heekeren, H. R., Abutalebi, J., Cappa, S. F., Villringer, A., & Perani, D. (2003). Early setting of grammatical processing in the bilingual brain. Neuron, 37, 159–170. Zou, L., Abutalebi, J., Zinszer, B., Yan, X., Shu, H., Peng, D., et al. (2012). Second language experience modulates functional brain network for the native language production in bimodal bilinguals. NeuroImage, 62, 1367–1375. Zou, L., Ding, G., Abutalebi, J., Shu, H., & Peng, D. (2012). Structural plasticity of left caudate in bimodal bilinguals. Cortex, 48, 1197–1206.
Introduction The human brain not only has evolved to accommodate a single language but also is, in fact, suited to acquire more than one language, such as the case of bilingual and multilingual individuals. As globalization advances, more people become bilingual or multilingual thus establishing bilingualism as the standard rather than the exception (Grosjean & Li, 2013). A bilingual individual may achieve different levels of proficiency in the two languages, using both languages in different contexts, by learning a new language following educational requirements, immigration, or alternative circumstances. By this definition, a bilingual individual is not only necessarily someone who has acquired both languages from birth, or early in life, but also that one who learns a second language (L2) later in life. The different contexts and circumstances of L2 acquisition have important effects upon the cerebral organization of multiple languages. Moreover, having acquired more than one language, the bilingual or multilingual speaker may eventually encounter potential conflicts between said languages, such as how to speak in one language while avoiding potential intrusions from the other. As a broad definition, the concept of neural representation of bilingualism refers to functional and structural neuroimaging evidence that provided the cerebral organization of two (or more) languages. These studies focus on not only how two or more languages are anatomically represented in the human brain, according to crucial variables such as proficiency, age of acquisition (AOA), and exposure, but also, ultimately, how individuals acquire, process, and eventually may later lose such languages. From a historical viewpoint, the landmark study of Pitres (1895) marked the initiation of this field and has enticed the interest of researchers for more than a century. Pitres in 1896 described cases of selective loss and recovery of a given language in bilingual aphasics, thus giving rise to vivid discussions about different potential neural locations for languages. Indeed, prior to the advent of functional neuroimaging, it was widely believed that bilingual language representation was assigned to different brain areas or even different hemispheres (Albert & Obler, 1978). This hypothesis was essentially based on the common observation of bilingual aphasics who recover only one language after stroke, while the other is lost; this led researchers to believe that the brain regions responsible for one language was damaged though the others remained intact. However, functional neuroimaging studies have so far contradicted this assumption (see, for review, Abutalebi, 2008; Indefrey, 2006; Perani & Abutalebi, 2005). Today, it is well established that bilinguals use the same neural substrate, thus identical brain structures for both languages. The neural networks can vary according to variables that influence neural plasticity, among those, the exposure or amount of use to a given language.
Brain Mapping: An Encyclopedic Reference
In this article, we will provide a brief overview of how two or more languages are organized in the human brain and what mediates their processes.
The Neural Representation of L2 For successful acquisition of an L2, an entire new set of phonological, lexico-semantic, and morphosyntactic knowledge, which is largely distinctive from the first language (L1), needs to be mentally stored and instantiated. In the case of L1 acquisition, the shaping and organization of such linguistic knowledge usually lead to a fairly effortless tuning of all cognitive processes subtending language. The same phenomenon manifests when an L2 is learned from birth or very early in life (i.e., before age 6) (Wartenburger et al., 2003). However, this rarely occurs for an L2 learned after early childhood. A crucial question to unravel is whether L2 learning is constrained by the ‘critical time period’ that is paralleled in neural terms with maturational changes in the brain (McDonald, 2000). According an influential account, that is, the critical period hypothesis (CPH) (Birdsong, 2006; Johnson & Newport, 1989), there is a critical period in acquiring full competence (phonological, lexico-semantic, and morphosyntactic representations) in two (or more) languages. On this basis, researchers have hypothesized a fundamental difference between L1 acquisition and L2 learning.
Neural Representation of L2 Grammar The aforementioned CPH hypothesizes the existence of a purported critical period for acquisition of phonology, morphology, and syntax (Birdsong, 2006; Johnson & Newport, 1989). In the case of morphology and syntax, the declarative/procedural model (DP) (Ullman, 2001) attempted to provide a rationale for putative differences. DP claims that in normal monolinguals, words are represented in a declarative (i.e., explicit) memory system, whereas grammatical rules are represented through a cognitive system that mediates the use of procedural memory (i.e., implicit memory processed without conscious awareness). Following the DP model, when an L2 is learned after the critical period, it can no longer rely on the procedural/implicit resources that are used for L1 grammatical processes. Rather, grammatical knowledge in L2 would be processed using explicit resources (much like L1 and L2 words). Furthermore, since procedural knowledge and declarative knowledge are mediated by distinct neural systems (i.e., Broca’s area and the basal ganglia and left temporal areas, respectively), late L2 learners would rely more heavily on posterior brain areas, (left temporal areas responsible for lexicosemantic processing and hence declarative knowledge) when
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compared with L1 speakers (Broca’s area and the basal ganglia), when computing L2 grammar (Ullman, 2001). It is worth emphasizing that functional neuroimaging studies have, so far, contradicted this assumption (see for review Abutalebi, 2008). Crucially, Sakai, Miura, Narafu, and Muraishi (2004) reported that the acquisition of grammatical competences in late bilingual twins is achieved through the same neural structures used in processing L1 grammar, that is, Broca’s area. Likewise, in an fMRI study investigating L2 verb conjugation (Sakai et al., 2004) and past tense word processing (Tatsuno & Sakai, 2005), increased activity in the areas mediating L1 syntax (i.e., Broca’s area) was reported, but not in posterior brain areas, as postulated by the DP model. Additional evidence was reported in studies investigating artificial grammar learning (Friederici, Bahlmann, Helm, Schubotz, & Anwander, 2006; Opitz & Friederici, 2004); acquisition of language-like rules of an artificial language was associated with increased recruitment of Broca’s area. These results support the notion that learning L2 grammar (albeit an artificial one) is carried out through the preexisting neural network that mediates native language grammar. As to the precise network mediating syntax in monolinguals, Friederici (2011) reported that syntactical processes are carried out by the frontal operculum (FOp) along with the anterior part of the superior temporal gyrus (STG). This network is responsible for both natural grammar processing in monolinguals and artificial grammar processing. However, as Friederici (2011) underlined, under less proficient processing conditions such as language learning in developmental ages or L2 learning, the network comprises not only the FOp an STG but also Broca’s area and surrounding areas and potentially also the basal ganglia. L2 grammar learning usually arises in the context of an already-specified language system (i.e., L1). Since the neural system underlying grammatical processes, including Broca’s area, has learned to compute grammatical processing for the native language (L1) during the developmental stages, it is likely that the same kind of neural computation is valid also for an eventual L2. Differences may arise in the initial stages of L2 learning, where a need of additional brain substrate for processing the newly learned L2 is required; but these neural differences seem to vanish once the proficiency becomes comparable to that of L1 (Consonni et al., 2013). In this specific case, the neural representation of L2 converges to that of L1, as suggested by Green (2003). As shown by functional neuroimaging, there is more brain activity for an L2 (especially when processed with a nonnative-like proficiency) in Broca’s area and surrounding regions. Following Indefrey (2006), bilinguals might compensate for lower efficiency in L2 by involving these regions more strongly.
Neural Representation of L2 Phonology Similar to grammar processing, critical periods have been postulated for phonological processing (Singleton, 2005). Correctly perceiving and producing the foreign language sounds are challenging tasks. Problems of this kind are reported even for individuals who have been exposed for considerable periods of time to an L2 (Pallier, Bosch, & SebastianGalle´s, 1997).
From a neuroanatomical perspective, phonetic perception and production appear to be carried out through specialized networks in the left hemisphere, such as Wernicke’s area, the left inferior parietal lobe, and Broca’s area, as shown by functional neuroimaging (De´monet, Thierry, & Cardebat, 2005). Again, one may pose the question as to whether L2 phonological representations are acquired, stored, and processed in a different fashion from that of the native language. Again, neuroimaging studies consistently provide evidence for a shared neural network for L1 and L2 phoneme perception and production (e.g., Heim & Friederici, 2003). Although the functional neuroimaging literature on phonological processing in bilinguals is rather limited (as compared to the many studies investigating morphosyntactic and lexico-semantic processing), some conclusions may be drawn: the available evidence shows that L2 phonology is essentially acquired and processed through the same neural structures mediating L1 phonology, that is, a network comprising the FOp, the supramarginal gyrus, and the left putamen. Some neuroimaging studies showed an increased extension of brain activity, indicating that overall L2 processing requires greater recruitment of neural resources. One reason for this observation might be that these studies have included late and low-proficiency L2 learners (i.e., Callan, Jones, Callan, & Yamada, 2004; Callan et al., 2003; Wang, Xue, Chen, Xue, & Dong, 2007) or monolingual subjects who, for the experimental purpose, were asked to learn phonetic contrasts in a foreign language (Golestani & Zatorre, 2004). In the latter case, it is possible that the greater brain activity may reflect the accommodation of a new set of sounds by the existing native speech system rather than the acquisition of a nonnative phonetic contrast in an L2 context. In the former case (i.e., L2 English speakers), it is plausible that processing sounds in L2, subserved by less calibrated representations, may require greater cognitive effort and therefore greater neuronal activity than processing sounds in L1.
Neural Representation of L2 Lexico-Semantics In the context of the lexico-semantic domain, the most influential cognitive model, that is, the revised hierarchical (RH) model (Kroll & Stewart, 1994), claims that separate lexical memory systems contain words for each of the two languages, whereas semantic concepts are stored in an abstract memory system common to both languages. Following this account, at the beginning stage of L2 acquisition, L2–L1 mediation would mainly occur between direct translations at the lexical level (i.e., L2 words are mentally translated into L1 words). However, with increasing L2 proficiency, L2 words would become more tightly bound to their specific conceptual representations and would be less dependent upon their L1 translation equivalent. Notably, following the RH model, lexical processing would be independent of the AOA of L2 and critical periods but would rather rely mostly on language proficiency. This is in line with Green’s convergence theory (2003) that postulates that many of the qualitative differences between native and L2 speakers disappear as proficiency increases. Regarding the neuroanatomical basis of the lexico-semantic system in bilinguals, functional neuroimaging studies, at the single word level, such as picture naming, verbal fluency, word completion, and word repetition tasks, have been consistently
INTRODUCTION TO COGNITIVE NEUROSCIENCE | Bilingualism
reported that L1 and L2 entail common neural activations in the left frontal and temporoparietal brain areas. This is true when the degree of L2 proficiency is comparable to L1 (Abutalebi, 2008). There are exceptions for bilinguals with different alphabetic scripts and bimodal bilinguals (see the succeeding text). Notably, these networks are identical to those commonly engaged when monolinguals perform the same kind of language tasks. On the other hand, bilinguals with low proficiency and/or low exposure to L2 engaged additional brain activity (Perani et al., 2003). At the single word level, the pattern of brain activation for L1 and L2 seems to converge; however, brain activation for more complex comprehension processes, such as sentencelevel comprehension, shows differences associated with the eventual workload of the task. Differences in brain activation between L1 and L2 have been found as more extended activations in prefrontal regions with increased cognitive workload in a listening comprehension task (Hasegawa, Carpenter, & Just, 2002) and in a frontal–parietal network related to phonological processes in a reading comprehension task (Buchweitz, Mason, Hasegawa, & Just, 2009). Studies also showed recruitment of additional brain networks to accommodate the processing demands of different writing conventions (different writing systems and scripts such as English and Chinese) (Perfetti et al., 2007; Tan et al., 2001). Hence, the level of dynamic distribution of brain activity in L2 compared with L1 is accounted for not only the differences in degrees of L2 proficiency but also the workload and eventually the linguistic distance. Interestingly, in addition to different activation associated with proficiency, workload, and orthographic systems, it is important to underline that the investigation of bimodal bilinguals (signed and spoken languages) may further widen our knowledge into converging processes across languages: in the
special case of bimodal bilinguals, processes associated with different languages conveyed in different modalities. A recent study showed that despite large similarities in the brain activation associated with spoken and sign-language production, bimodal bilinguals, in comparison with monolinguals, showed more right-hemisphere temporal and occipital activation during a sign-language task. The additional righthemisphere areas recruited may support cognitive processes specifically associated with sign-language production (Zou, Ding, Abutalebi, Shu, & Peng, 2012; Zou, Abutalebi, et al., 2012).
Language Control and Neural Consequences Induced by Bilingualism Common to the aforementioned studies are the findings of additional brain activity during L2 processing as compared with L1 processing. This extra activity is usually reported when the level of proficiency of L2 is not native-like, or when the task load is different, or crucially when the amount of exposure to a given language varies. Indeed, recent studies have shown that even in early and high-proficiency bilinguals, the amount of exposure and usage of languages does result in differential activity (Abutalebi et al., 2007; Perani et al., 2003). As to the precise location of the extra activity, it is found mostly in the prefrontal areas (Abutalebi, 2008) and eventually also in the anterior cingulate cortex (ACC), the left inferior parietal lobule, and the left caudate (see Figure 1). Interestingly, this set of brain areas is usually linked to executive control and not specifically to language processing. Findings indicating that low-proficiency bilinguals rely on executive control areas when processing a weak L2 may suggest that they are in need of greater mental coordination in order to
preSMA /ACC
Pre frontal
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Figure 1 The language control network in bilinguals. Adapted from Abutalebi, J., & Green, D. (2007). Bilingual language production: The neurocognition of language representation and control. Journal of Neurolinguistics, 20, 242–275.
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speak an L2 unerringly. Abutalebi and Green (2007) referred to this processes as language control. Language control more precisely refers to the unique ability of bilinguals to suppress one language while speaking the other. This ability is strictly necessary for preventing that items of the language not in use slip into the language in use. However, the need to control and monitor the two languages may also induce a cost by increasing the effort bilinguals need to make especially in speech production tasks (Abutalebi & Green, 2007; Kroll, Bobb, Misra, & Guo, 2008). Consistent with this view, several investigations have shown a greater engagement of brain areas implicated in language control in bilinguals as compared with monolinguals. For example, Abutalebi and collaborators have convincingly argued that the head of the left caudate and the left ACC are especially recruited during bilingual language processing (Abutalebi et al., 2008; Abutalebi, Della Rosa, Ding, et al., 2013; Garbin et al., 2011), suggesting that such structures are crucially involved in keeping the two languages apart during language processing, at least in contexts in which both languages are engaged (see Zou, Ding, et al., 2012 for similar evidence with bimodal bilinguals). A very interesting recent discovery in this context is the fact that bilingualism induces also structural changes in the brain. Bilingualism induces experience-related structural changes (i.e., in terms of increased gray or white matter density) in the frontal lobes (Luk, Bialystok, Craik, & Grady, 2011), the left inferior parietal lobule (Della Rosa et al., 2013; Mechelli et al., 2004), the ACC (Abutalebi et al., 2012), and subcortical structures such as the left caudate (Zou, Ding, et al., 2012) and left putamen (Abutalebi, Della Rosa, Castro Gonzaga, et al., 2013). These areas are part of the executive control network and the reason why bilinguals usually have a cognitive advantage in executive control tasks over monolinguals; that is, bilinguals are faster to resolve cognitive conflicts than monolinguals (Bialystok, Craik, & Luk, 2012). Noteworthy, a relevant direct consequence of these structural changes in the executive control network is the promotion of cognitive reserve in elderly people: elderly bilinguals outperform monolinguals in executive control tasks and appear to have a 4–5-year onset delay of behavioral symptoms associated to neurodegenerative diseases such dementia as compared with monolinguals (Alladi et al., 2013; Bialystok et al., 2012).
See also: INTRODUCTION TO ANATOMY AND PHYSIOLOGY: Lateral and Dorsomedial Prefrontal Cortex and the Control of Cognition; INTRODUCTION TO CLINICAL BRAIN MAPPING: Disorders of Language; INTRODUCTION TO COGNITIVE NEUROSCIENCE: The Neurobiology of Sign Language; INTRODUCTION TO SYSTEMS: Grammar and Syntax.
References Abutalebi, J. (2008). Neural processing of second language representation and control. Acta Psychologica, 128, 466–478. Abutalebi, J., Annoni, J. M., Seghier, M., Zimine, I., Lee-Jahnke, H., Lazeyras, F., et al. (2008). Language control and lexical competition in bilinguals: An event-related fMRI study. Cerebral Cortex, 18, 1496–1505. Abutalebi, J., Brambati, S. M., Annoni, J. M., Moro, A., Cappa, S. F., & Perani, D. (2007). The neural cost of the auditory perception of language switches: An eventrelated fMRI study in bilinguals. Journal of Neuroscience, 27, 13762–13769.
Abutalebi, J., Della Rosa, P. A., Castro Gonzaga, A., Keim, R., Costa, A., & Perani, D. (2013). The role of the left putamen in multilingual language production. Brain and Language, 125, 307–315. Abutalebi, J., Della Rosa, P. A., Ding, G., Weekes, B. S., Costa, A., & Green, D. W. (2013). Language proficiency modulates the engagement of cognitive control areas in multilinguals. Cortex, 49, 905–911. Abutalebi, J., Della Rosa, P. A., Green, D. W., Hernandez, M., Scifo, P., Keim, R., et al. (2012). Bilingualism tunes the anterior cingulate cortex for conflict monitoring. Cerebral Cortex, 22, 2076–2086. Abutalebi, J., & Green, D. (2007). Bilingual language production: The neurocognition of language representation and control. Journal of Neurolinguistics, 20, 242–275. Albert, M. L., & Obler, L. K. (1978). The bilingual brain. New York: Academic Press. Alladi, S., Bak, T. H., Duggirala, V., Surampudi, B., Shailaja, M., Kumar Shukla, A., et al. (2013). Bilingualism delays age at onset of dementia, independent of education and immigration status. Neurology, 81, 1938–1944. Bialystok, E., Craik, F. I., & Luk, G. (2012). Bilingualism: Consequences for mind and brain. Trends in Cognitive Sciences, 16, 240–250. Birdsong, D. (2006). Age and second language acquisition and processing: A selective overview. Language Learning, 56, 9–49. Buchweitz, A., Mason, R. A., Hasegawa, M., & Just, M. A. (2009). Japanese and English sentence reading comprehension and writing systems: An fMRI study of first and second language effects on brain activation. Bilingualism: Language and Cognition, 12, 141–151. Callan, D. E., Jones, J. A., Callan, A. K., & Yamada, R. A. (2004). Phonetic perceptual identification by native- and second-language speakers differentially activates brain regions involved with acoustic phonetic processing and those involved with articulatory–auditory/orosensory internal models. NeuroImage, 22, 1182–1194. Callan, D. E., Tajima, K., Callan, A. M., Kubo, R., Masaki, S., & Akahane-Yamada, R. (2003). Learning-induced neural plasticity associated with improved identification performance after training of a difficult second language phonetic contrast. NeuroImage, 19, 113–124. Consonni, M., Cafiero, R., Marin, D., Tettamanti, M., Iadanza, A., Fabbro, F., et al. (2013). Neural convergence for language comprehension and grammatical class production in highly proficient bilinguals is independent of age of acquisition. Cortex, 49, 1252–1258. Della Rosa, P. A., Videsott, G., Borsa, V. M., Canini, M., Weekes, B., Franceschini, R., et al. (2013). A neural interactive landmark for multilingual talent. Cortex, 49, 605–608. De´monet, J. F., Thierry, G., & Cardebat, D. (2005). Renewal of the neurophysiology of language: Functional neuroimaging. Physiological Reviews, 85, 49–95. Friederici, A. D. (2011). The brain basis of language processing: From structure to function. Physiological Reviews, 91, 1357–1392. Friederici, A. D., Bahlmann, J., Helm, S., Schubotz, R. I., & Anwander, A. (2006). The brain differentiates human and non-human grammars: Functional localization and structural connectivity. Proceedings of the National Academy of Sciences of the United States of America, 103, 2458–2463. Garbin, G., Costa, A., Sanjuan, A., Forn, C., Rodriguez-Pujadas, A., Ventura, N., et al. (2011). Neural bases of language switching in high and early proficient bilinguals. Brain and Language, 119, 129–135. Golestani, N., & Zatorre, R. J. (2004). Learning new sounds of speech: Reallocation of neural substrates. NeuroImage, 21, 494–506. Green, D. W. (2003). The neural basis of the lexicon and the grammar in L2 acquisition. In R. van Hout, A. Hulk, F. Kuiken, & R. Towell (Eds.), The interface between syntax and the lexicon in second language acquisition. Amsterdam: John Benjamins. Grosjean, F., & Li, P. (2013). The psycholinguistics of bilingualism. New York: Wiley. Hasegawa, M., Carpenter, P., & Just, M. A. (2002). An fMRI study of bilingual sentence comprehension and workload. NeuroImage, 15, 647–660. Heim, S. T., & Friederici, A. D. (2003). Phonological processing in language production: Time course of brain activity. NeuroReport, 14, 2031–2033. Indefrey, P. (2006). A meta-analysis of hemodynamic studies on first and second language processing: Which suggested differences can we trust and what do they mean? Language Learning, 56, 279–304. Johnson, J. S., & Newport, E. L. (1989). Critical period effects in second language learning: The influence of maturational state on the acquisition of English as a second language. Cognitive Psychology, 21, 60–99. Kroll, J. F., Bobb, S. C., Misra, M., & Guo, T. (2008). Language selection in bilingual speech: Evidence for inhibitory processes. Acta Psychologica, 128, 416–430. Kroll, J. F., & Stewart, E. (1994). Category interference in translation and picture naming: Evidence for asymmetric connections between bilingual memory. Journal of Memory and Language, 33, 149–174. Luk, G., Bialystok, E., Craik, F., & Grady, C. (2011). Lifelong bilingualism maintains white matter integrity in older adults. Journal of Neuroscience, 31, 16808–16813.
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McDonald, J. (2000). Grammaticality judgments in a second language: Influences of age of acquisition and native language. Applied Psycholinguistics, 21, 395–423. Mechelli, A., Crinion, J. T., Noppeney, U., O’Doherty, J., Ashburner, J., Frackowiack, R. S., et al. (2004). Neurolinguistics: Structural plasticity in the bilingual brain. Nature, 431, 757. Opitz, B., & Friederici, A. D. (2004). Interactions of the hippocampal system and the prefrontal cortex in learning language-like rules. NeuroImage, 19, 1730–1737. Pallier, C., Bosch, L., & Sebastian-Galle´s, N. (1997). A limit on behavioral plasticity in speech perception. Cognition, 64, 9–17. Perani, D., & Abutalebi, J. (2005). Neural basis of first and second language processing. Current Opinion in Neurobiology, 15, 202–206. Perani, D., Abutalebi, J., Paulesu, E., Scifo, P., Cappa, S. F., & Fazio, F. (2003). The role of language dominance and usage in early high proficient bilinguals. Human Brain Mapping, 19, 170–182. Perfetti, C., Liu, Y., Fiez, J., Nelson, J., Bolger, D. J., & Tan, L.-H. (2007). Reading in two writing systems: Accommodation and assimilation of the brain’s reading network. Bilingualism: Language and Cognition, 10, 131. Pitres, A. (1895). Etude sur l’aphasie chez les polyglottes. Revue de me´decine, 15, 873–899. Sakai, K. L., Miura, K., Narafu, N., & Muraishi, Y. (2004). Correlated functional changes of the prefrontal cortex in twins induced by classroom education of second language. Cerebral Cortex, 14, 1233–1239.
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Singleton, D. (2005). The critical period hypothesis: A coat of many colours. International Review of Applied Linguistics in Language Teaching, 43, 269–285. Tan, L. H., Liu, H. L., Perfetti, C. A., Spinks, J. A., Fox, P. T., & Gao, J. H. (2001). The neural system underlying Chinese logograph reading. NeuroImage, 13, 836–846. Tatsuno, Y., & Sakai, K. L. (2005). Language related activations in the left prefrontal regions are differentially modulated by age, proficiency and task demands. Journal of Neuroscience, 16, 1637–1644. Ullman, M. T. (2001). A neurocognitive perspective on language: The declarative/ procedural model. Nature Reviews. Neuroscience, 2, 717–726. Wang, Y., Xue, G., Chen, C., Xue, F., & Dong, Q. (2007). Neural bases of asymmetric language switching in second-language learners: An ER-fMRI study. NeuroImage, 35, 862–870. Wartenburger, I., Heekeren, H. R., Abutalebi, J., Cappa, S. F., Villringer, A., & Perani, D. (2003). Early setting of grammatical processing in the bilingual brain. Neuron, 37, 159–170. Zou, L., Abutalebi, J., Zinszer, B., Yan, X., Shu, H., Peng, D., et al. (2012). Second language experience modulates functional brain network for the native language production in bimodal bilinguals. NeuroImage, 62, 1367–1375. Zou, L., Ding, G., Abutalebi, J., Shu, H., & Peng, D. (2012). Structural plasticity of left caudate in bimodal bilinguals. Cortex, 48, 1197–1206.