Peer Reviewed Articles Summary (BILINGUALISM AND LANGUAGE DISORDERS IN BILINGUALS)

Feature Review

Bilingualism: consequences for mind and brain Ellen Bialystok1,2, Fergus I.M. Craik2 and Gigi Luk3

1 Department of Psychology, York University, 4700 Keele Street, Toronto, ON, M3J 1P3, Canada

2 Rotman Research Institute of Baycrest, 3560 Bathurst Street, Toronto, ON, M6A 2E1,Canada

3 Harvard Graduate School of Education, 14 Appian Way, Cambridge, MA 02138, USA

Review

Building on earlier evidence showing a beneficial effect of bilingualism on children’s cognitive development, we review recent studies using both behavioral and neuro- imaging methods to examine the effects of bilingualism on cognition in adulthood and explore possible mecha- nisms for these effects. This research shows that bilin- gualism has a somewhat muted effect in adulthood but a larger role in older age, protecting against cognitive decline, a concept known as ‘cognitive reserve’. We discuss recent evidence that bilingualism is associated with a delay in the onset of symptoms of dementia. Cognitive reserve is a crucial research area in the context of an aging population; the possibility that bilingualism contributes to cognitive reserve is therefore of growing importance as populations become increasingly diverse.

Why bilingualism? It is generally believed that more than half of the world’s population is bilingual [1]. In each of the U.S.A.1 and Canada2, approximately 20% of the population speaks a language at home other than English. These figures are higher in urban areas, rising to about 60% in Los Angeles3

and 50% in Toronto4. In Europe, bilingualism is even more prevalent: in a recent survey, 56% of the population across all European Union countries reported being functionally bilin- gual, with some countries recording particularly high rates, such as Luxembourg at 99%5. Bilinguals, therefore, make up a significant portion of the population. Importantly, accumulating research shows that the development, efficien-

Corresponding author: Bialystok, E. ([email protected]) 1 U. S. Census Bureau (2010) The 2011 Statistical Abstract. Languages Spoken at

Home by Language: 2008, Table 53. Retrieved August 4, 2011 from http://www.census. gov/compendia/statab/cats/population/ancestry_language_spoken_at_home.html.

2 Statistics Canada (2007) 2006 Census of Canada highlight tables: Population by language spoken most often at home and age groups, 2006 counts, for Canada, provinces and territories – 20% sample data. (Catalogue number 97-555-XWE2006002). Retrieved August 4, 2011 from http://www12.statcan.ca/census-recensement/2006/dp-pd/hlt/ 97-555/T402-eng.cfm?Lang=E&T=402&GH=4&SC=1&S=99&O=A.

3 U. S. Census Bureau (2010) The 2011 Statistical Abstract. Language Spoken at Home – Cities With 100,000 Persons or More: 2008, Table 55. Retrieved August 4, 2011 from http://www.census.gov/compendia/statab/cats/population/ancestry_language_ spoken_at_home.html.

4 Statistics Canada (2007) 2006 Census of Canada highlight tables: Population by language spoken most often at home and age groups, 2006 counts, for Canada, provinces and territories – 20% sample data. (Catalogue number 97-555-XWE2006002). Retrieved August 4, 2011 from http://www12.statcan.ca/census-recensement/2006/dp-pd/hlt/ 97-555/T402-eng.cfm?Lang=E&T=402&GH=4&SC=1&S=99&O=A.

5 European Commission (2006) ‘Special Eurobarometer 243: Europeans and their Languages (Executive Summary)’ (PDF). Europa web portal. p. 3. Retrieved Novem- ber 1, 2011 from http://ec.europa.eu/public_opinion/archives/ebs/ebs_243_sum_en.pdf.

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cy, and decline of crucial cognitive abilities are different for bilinguals than for monolinguals. What are these cognitive differences and how does bilingualism lead to these changes?

The context for examining how bilingualism affects cog- nitive ability is functional neuroplasticity, that is, the study of how experience modifies brain structure and brain func- tion. Such modifications have been found following experi- ences as diverse as juggling [2], video-game playing [3], careers in architecture [4], taxi-driving [5], and musical training [6,7]. Bilingualism is different from all of these: like juggling and playing video games, it is intense, and, like architecture and driving taxis in London, it is sustained, but, unlike these experiences, bilinguals are not typically pre- selected for talent or interest. Although bilinguals undoubt- edly differ from monolinguals in certain ways, they gener- ally did not choose bilingualism. Rather, the circumstances of their family, place of birth, or immigration history simply required that they learn more than one language.

What is different about bilingual minds? It has long been assumed that childhood bilingualism affected developing minds, but the belief was that the consequences for children were negative: learning two languages would be confusing [8]. A study by Peal and Lambert [9] cast doubt on this belief by reporting that children in Montreal who were either French-speaking monolinguals or English–French bilinguals performed dif- ferently on a battery of tests. The authors had expected to find lower scores in the bilingual group on language tasks but equivalent scores in non-verbal spatial tasks, but instead found that the bilingual children were superior on most tests, especially those requiring symbol manipu- lation and reorganization. This unexpected difference be- tween monolingual and bilingual children was later explored in studies showing a significant advantage for bilingual children in their ability to solve linguistic prob- lems based on understanding such concepts as the differ- ence between form and meaning, that is, metalinguistic awareness [10–16] and non-verbal problems that required participants to ignore misleading information [17,18].

Research with adult bilinguals built on these studies with children and reported two major trends. First, a large body of evidence now demonstrates that the verbal skills of bilinguals in each language are generally weaker than are those for monolingual speakers of each language.

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Considering simply receptive vocabulary size, bilingual children [19] and adults [20] control a smaller vocabulary in the language of the community than do their monolingual counterparts. On picture-naming tasks, bilingual partici- pants are slower [21–24] and less accurate [25,26] than monolinguals. Slower responses for bilinguals are also found for both comprehending [27] and producing words [28], even when bilinguals respond in their first and dominant lan- guage. Finally, verbal fluency tasks are a common neuro- psychological measure of brain functioning in which participants are asked to generate as many words as they can in 60 s that conform to a phonological or semantic cue. Performance on these tasks reveals systematic deficits for bilingual participants, particularly in semantic fluency con- ditions [29–33], even if responses can be provided in either language [34]. Thus, the simple act of retrieving a common word is more effortful for bilinguals.

In contrast to this pattern, bilinguals at all ages demon- strate better executive control than monolinguals matched in age and other background factors. Executive control is the set of cognitive skills based on limited cognitive resources for such functions as inhibition, switching attention, and work- ing memory [35]. Executive control emerges late in develop- ment and declines early in aging, and supports such activities as high-level thought, multi-tasking, and sustained atten- tion. The neuronal networks responsible for executive control are centered in the frontal lobes, with connections to other brain regions as necessary for specific tasks. In children, executive control is central to academic achievement [36], and, in turn, academic success is a significantpredictor of long term health and well being [37]. In a recent meta-analysis, Adesope et al. [38] calculated medium to large effect sizes for the executive control advantages in bilingual children, and Hilchey and Klein [39] summarized the bilingual advantage over a large number of studies with adults. This advantage has been shown to extend into older age and protect against cognitive decline [21,40,41], a point to which we turn below.

In this review, we examine the evidence for bilingual advantages in executive control and explore the possible mechanisms and neural correlates that may help to ex- plain them. Our conclusion is that lifelong experience in managing attention to two languages reorganizes specific brain networks, creating a more effective basis for execu- tive control and sustaining better cognitive performance throughout the lifespan.

Language processing in bilinguals Joint activation of languages

A logical possibility for the organization of a bilingual mind is that it consists of two independently-represented lan- guage systems that are uniquely accessed in response to the context: a fluent French–English bilingual ordering coffee in a Parisian café has no reason to consider how to form the request in English, and a Cantonese–English bilingual studying psychology in Boston does not need to recast the material through Chinese. Yet, substantial evi- dence shows that this is not how the bilingual mind is organized. Instead, fluent bilinguals show some measure of activation of both languages and some interaction between them at all times, even in contexts that are entirely driven by only one of the languages.

The evidence for this conclusion comes from psycholin- guistic studies using such tasks as cross-language priming (in which a word in one language facilitates retrieval of a semantically related word in the other language) and lexical decision (in which participants decide whether a string of letters is an actual word in one of the languages) that show the influence of the currently unused language for both comprehension and production of speech [42–48]. Further evidence comes from patient studies showing intrusions from the irrelevant language or inappropriate language switches [49], and imaging studies indicating involvement of the non-target language while performing a linguistic task in the selected language [50–52]. Using eye-tracking technology, for example, Marian, Spivey, and Hirsch [53] reported that English–Russian bilinguals per- forming a task in English in which they had to look at the named picture from four alternatives were distracted by a picture the name of which shared phonology with Russian, even though there was no connection to the meaning of the target picture and no contextual cues indicating that Rus- sian was relevant. Similarly, Thierry and Wu [54] pre- sented English monolinguals, Chinese–English bilinguals, and Chinese monolinguals with pairs of words in English (translated to Chinese for Chinese monolinguals) and asked participants to decide if the words were semantically related or not. The manipulation was that half of the pairs contained a repeated character in the written Chinese forms, even though that orthographic feature was unrelat- ed to the English meaning. Waveforms derived from anal- yses of electroencephalography (EEG) are used to indicate the neuronal response to language on a millisecond by millisecond scale. An event-related potential (ERP) called the N400 (i.e. a negative-going waveform peaking approxi- mately 400 msec after the onset of a target stimulus) signals the effort associated with integrating the meaning of words. The more similar the words are to each other, the smaller is the amplitude of the N400. In the study by Thierry and Wu, semantic relatedness was associated with significantly smaller N400 amplitude in all groups as expected, but the repeated character also led to smaller N400 for the two Chinese groups. Thus, although irrele- vant to the task, participants were accessing the Chinese forms when making judgments about the semantic relation between English words. Subsequent research has refined these results by showing their basis in the phonology rather than the orthography of spoken language [55] and extended the phenomenon to the phonological hand forms of American Sign Language [56].

This joint activation is the most likely mechanism for understanding the consequences of bilingualism for both linguistic and non-linguistic processing. For linguistic pro- cessing, joint activation creates an attention problem that does not exist for monolinguals: in addition to selection constraints on such dimensions as register, collocation, and synonymy, the bilingual speaker also has to select the correct language from competing options. Although joint activation creates a risk for language interference and language errors, these rarely occur, indicating that the selection of the target language occurs with great accuracy. However, this need to select at the level of language system makes ordinary linguistic processing more effortful for

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bilinguals than monolinguals and explains some of the costs in psycholinguistic studies described above. For non-linguistic processing, the need to resolve competition and direct attention is primarily the responsibility of gen- eral cognitive systems, in particular executive functions. The possible influence of linguistic processes on non-lin- guistic executive control has significant consequences for lifespan cognition and is discussed in the next section.

Consequences of joint activation

An appealing suggestion for how the executive control system achieves linguistic selection in the context of joint activation is through inhibition of the non-target language. At least two influential models have been proposed that place inhibition at the center of this selection. The first, the Inhibitory Control model [57] is based on the Supervisory Attentional System [58] and extends a domain-general and resource-limited attention system to the management of competing languages. The second, the Bilingual Interac- tive Activation Model (BIA+) [59], uses computer simula- tion to model lexical selection from both intralingual and extralingual competitors. Although both models assign a primary role to inhibition, they are very different from each other and address a different aspect of the selection prob- lem. It is useful, therefore, to consider the distinction between global inhibition and local inhibition proposed by De Groot and Christoffels [60]. Global inhibition refers to suppression of an entire language system, as in inhibit- ing French when speaking English, and local inhibition refers to inhibition of a specific competing distractor, such as the translation equivalent of the required concept. Both processes are required for fluent language selection but the two are carried out differently. Guo, Liu, Misra, and Kroll [61] used functional magnetic resonance imaging (fMRI) to demonstrate the recruitment of different systems for each of global inhibition (dorsal left frontal gyrus and parietal cortex) and local inhibition (dorsal anterior cingulate cor- tex, supplementary motor area) in a sample of Chinese– English bilinguals, and validated their distinct roles in bilingual language control. Although Green’s inhibitory control model is consistent with both types of inhibition, Dijkstra’s BIA+ model is limited to modeling item selection in local inhibition.

These types of inhibition also differ in their primary domain of influence, with local inhibition largely affecting linguistic performance and global inhibition affecting both linguistic and cognitive performance. The linguistic out- comes of inhibition are reduced speed and fluency of lexical access for bilinguals as described above. However, perfor- mance also requires a selection bias towards the target language, showing a role for activation [62,63] as well as inhibition. These alternatives are not mutually exclusive but indicate the need for a more complete description of how attention is managed in bilingual language proces- sing. Ultimately the degree of both inhibition and activa- tion are relative rather than absolute and will be modulated by contextual, linguistic, and cognitive factors. The cognitive outcomes of linguistic inhibition are en- hanced attentional control and will be described more fully in the next section. Importantly, the cognitive and linguis- tic outcomes are related. Three studies have reported a

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relationship between inhibition and ability in verbal and non-verbal tasks by showing a correlation between Stroop task performance and competing word selection [64], Si- mon task performance and language switching in picture naming [65], and cross-language interference and a variety of executive control measures [66]. Such results point to an extensive reorganization of cognitive and linguistic pro- cesses in bilinguals.

Cognitive networks in bilinguals Bilingual performance on conflict tasks

Early evidence that bilingual children solved non-verbal conflict tasks differently from monolingual children was reported in a study by Bialystok and Majumder [17]. Eight- year-old children were given a variety of non-verbal problems to solve, some of which contained perceptual distraction (block design from the Wechsler Intelligence Scale for Children, WISC [67]) and some which did not (Noelting’s Juice Task [68,69]). Bilingual children outper- formed monolinguals on the conflict tasks, but children in the two groups were comparable on tasks that did not include distracting perceptual information. This pattern has been confirmed in studies of both children and adults using a flanker task (children: [70,71]), theory of mind task (children: [72,73]; adults: [74]), Simon task (children: [75]; adults: [40]). Other studies with adults have shown better performance by bilinguals in naming the font color in a Stroop task [21], smaller costs in task switching [76], better ability to maintain task set in an attention task [77], and more susceptibility to negative priming, presumably be- cause of greater inhibition [78].

Some studies have extended these bilingual advantages into older age. Bialystok, Craik, Klein and Viswanathan [40] reported an experiment in which middle-aged and older adults who were either monolingual or bilingual were given a version of the Simon task. Participants were shown either a green or a red square on each trial, and the task was to press an associated response key as rapidly as possible. The keys were located at each side of the presen- tation screen. In one condition, the squares appeared centrally on the screen, so there was no spatial conflict between the location of stimuli and responses; in this condition there were no reaction-time (RT) differences between language groups. In a second condition, the col- ored squares appeared laterally on the screen, either di- rectly above the appropriate response key (congruent condition) or on the other side of the screen, above the incorrect response key (incongruent condition). The RT difference between congruent and incongruent response trials (the Simon effect) is a measure of attentional control. Bilinguals produced smaller Simon effects than monolin- guals at all ages.

Three other results from this study are noteworthy. First, the decrease in attentional control in older adults was reduced in the bilingual groups, suggesting that bilin- gualism may be protective against the effects of cognitive aging. Second, whereas a bilingual advantage was expected for incongruent stimuli, it was also found for congruent stimuli. This result has been replicated in sub- sequent studies [39] and is difficult to account for in terms of response conflict or inhibition. Third, prolonged practice

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reduced both the Simon effect and the size of the bilingual advantage. Apparently all participants can learn to disre- gard the distracting effects of interfering stimuli given sufficient practice on a task, but it seems that bilinguals can learn this type of inhibition more rapidly. One inter- esting question in this regard is the extent to which this attenuation of attentional control is specific to the prac- ticed situation, or whether it generalizes to tasks tapping attentional control in a different manner. Our conjecture is that the attenuation effect is context specific.

A complication that has emerged as more results are reported is that the bilingual advantage is not always found in samples of young adults. For example, a study examining performance on the Simon task in 5-year-olds, young, middle-aged and older adults found a bilingual advantage in RT in the 5-year-olds and in the older adults, but not in the young adult group [79]. Similarly, a study of the Stroop effect in younger and older adults found a bilingual advantage in both age groups but when the same participants performed the Simon arrow task the bilingual advantage was found only in the older adults [21]. Simi- larly, Salvatierra and Rosselli [41] used a simple version of the Simon task and reported a bilingual advantage for older but not younger adults. There is thus some evidence that the bilingual advantage is greatest in children and in older adults, but less constantly present in young adults – perhaps because the young adult group is at the develop- mentally peak age for cognitive control.

It appears that bilingual advantages for young adults tend to emerge on tasks or conditions that are difficult. For example, Bialystok [80] found that bilingual young adults outperformed their monolingual counterparts on the direc- tional arrow Simon task, but only on the condition that included more monitoring and switching than a simpler condition. Similarly, several studies by Costa and collea- gues have reported a bilingual advantage in young adults [71,81,82] but only under some conditions. For example, Costa et al. [81] demonstrated that the bilingual advantage on a flanker task held only under high monitoring condi- tions. In versions where most of the trials were of one type (congruent or incongruent), no bilingual advantage was observed; the advantage was found, however, in a condition involving 25% incongruent and 75% congruent trials, al- though even there the advantage decreased over blocks of the experiment (cf. [44]). Costa et al. [81] concluded that the bilingual advantage reflects a more efficient monitoring system for conflict resolution, in that bilinguals may be better at determining when the misleading information can be safely ignored. Finally, Hernández et al. [82] used a non-linguistic version of the Stroop effect and found a trend towards both reduced interference and enhanced facilita- tion in young adult bilinguals compared with monolinguals (cf. older participants in [21]). One interesting aspect of the studies by Costa, Hernández and colleagues is that the monolinguals were Spanish speakers and the bilinguals’ two languages were Catalan and Spanish. Most of the participants were undergraduate students and were not immigrants, so the two groups were well equated apart from the language difference. In summary, the evidence for a bilingual advantage in younger adults is more sporadic than in other age groups, although at all ages there are

some reports of studies showing no difference between monolinguals and bilinguals performing a conflict task.

Neural correlates of cognitive reorganization

Recently, studies have begun to investigate the neural correlates of bilingual processing examined in the behav- ioral research. The majority of this research has used fMRI to study bilinguals performing a linguistic task in their two languages. Typically, participants name pictures or gener- ate words in response to a cue signaling the required language, and performance is compared for single lan- guage and mixed language conditions. Two early studies revealed promising results. The first led to the surprising finding that language switching was accompanied by acti- vation in the dorsolateral prefrontal cortex (DLPFC), an area known to be part of the general executive control system [24]. Less surprising was a study showing the involvement of Broca’s area as well as a left frontal area in a language switching task [83]. Subsequent re- search has corroborated the involvement of these systems and has shown that language switching elicits a spatially- distributed activation pattern involving bilateral frontal and precentral areas, bilateral caudate, bilateral (or mid- line) pre-supplementary areas (pre-SMA), and bilateral temporal regions. This pattern has been found for Ger- man-French bilinguals [84], Spanish-Catalan bilinguals [85], Chinese–English bilinguals [61,86,87] and Span- ish–English bilinguals [88]. A few studies [61,84] have also reported activation in anterior cingulate cortex (ACC), but activation in this area is not consistently observed. Abu- talebi and colleagues [89] extended this finding to show activation of ACC for both language switching and non- verbal switching. Importantly, these studies confirm that frontal systems involved in executive control are recruited by bilinguals to manage attention to language.

Abutalebi and Green [90] conducted a qualitative review of these studies and proposed that the ACC, left prefrontal cortex, left caudate and bilateral supramarginal gyri (SMG) constitute the neural correlates of the control mechanism for bilingual language production. This model was confirmed in a quantitative meta-analysis examining bilingual language switching [91] (Figure 1). Both the qualitative and quanti- tative analyses point to multiple cortical regions in which functional activity is altered by bilingualism, but an out- standing question is whether activity in these regions is synchronous, forming a neural network that is responsive to bilinguals’ experience of managing two languages. To this end, a study by Nakamura and colleagues [92] showed strong connectivity between left inferior frontal gyrus (IFG) and left middle temporal gyrus (MTG) in a group of Japanese–English bilinguals performing a cross-language priming task. The connectivity was stronger in the frontal- temporal coupling than in the reverse direction. This pat- tern was replicated using transcranial magnetic stimulation (TMS) with Japanese–English bilingual participants per- forming the same cross-language priming task. Nakamura and colleagues [92] interpreted the results as indicating top- down control from left IFG to left MTG in a bilingual context.

Taken together, fMRI research on bilingual language switching has implicated distributed cortical activation that converges in the frontal regions. Intriguingly, the

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Figure 1. Bilingual influence on brain function and structure. Transparent brains showing the left and right hemispheres. Green voxels depict grey matter regions showing

high activation during bilingual language switching in a meta-analysis [90]. Red–yellow voxels indicate regions of higher white matter integrity in bilingual older adults

relative to monolinguals [107]. Together, the functional and structural data indicate that neural correlates of bilingualism are observed in the frontal lobes, generally

responsible for higher cognition such as executive functions.

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brain regions related to bilingual switching are also critical for general attention and cognitive control [93,94]. This overlap in brain regions activated for bilingual switching and cognitive control implies that the same mechanisms may be involved in both activities, and that these shared processes might help to explain the superior performance of bilinguals on non-verbal conflict tasks. In other words, using these cognitive control networks for bilingual lan- guage processing may reconfigure them for other purposes, providing part of the explanation for the behavioral differ- ences between monolinguals and bilinguals found in non- verbal conflict tasks. Specifically, the evidence suggests that cognitive control networks may be more broadly based in bilinguals as a result of their dual function. However, fMRI studies on language switching in bilinguals can only show that these networks are included in bilingual lan- guage selection. Determining whether or not such recon- figuration occurs can only be evaluated by comparing monolinguals and bilinguals performing non-verbal con- flict tasks. The hypothesis is that monolinguals and bilin- guals will perform non-verbal control problems using somewhat different networks, specifically, that the net- work used by bilinguals will be more broadly based.

Only a few studies have contrasted the neural correlates of non-linguistic cognitive control in bilinguals and mono- linguals. Garbin and colleagues [95] gave a color-shape switching task to Spanish monolingual and Spanish- Catalan bilingual young adults in fMRI. A bivalent stimu- lus (e.g. a red circle) and a cue (e.g. ‘color’ or ‘shape’) were shown, and participants responded to the indicated dimen- sion. Both RT of switch costs and accuracy favored the bilingual participants, but activation patterns were also different for the two groups: monolinguals showed in- creased activation in the right IFG, whereas bilinguals showed increased activation in left inferior frontal gyrus. More interestingly, higher levels of activation in left IFG and left striatum were associated with smaller switch costs for the bilingual participants, but increased activation in the right IFG was associated with larger switch costs. In

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light of the lack of switching effect in the behavioral data, it is possible that the bilinguals relied more on the left IFG and striatum in face of the demand to switch between responses associated with a bivalent stimulus. The left IFG was identified in both the qualitative [90] and quanti- tative [91] meta-analyses of bilingual language switching. This region is central to speech production [96] and has been shown to have higher activation for bilinguals than monolinguals during speech production [97,98]. Thus, left IFG appears to be one of the overlapping brain regions in bilinguals handling both language switching and non-lin- guistic cognitive control.

A study by Luk and colleagues [99] used an adaptation of a flanker task to compare activation in monolingual and bilingual participants. The stimuli consisted of a string of five chevrons, and the task was to indicate the direction of the red one (that could appear in one of three positions) while ignoring the four black ones. In a previous behavioral study with these stimuli, bilinguals performed this task more rapidly than monolinguals [100]. The fMRI data were analyzed using a multivariate statistical technique for neuroimaging data (Partial Least Squares; for review, see [101]) to identify integrated neural networks. The results showed that monolinguals and bilinguals recruited different neural networks for both congruent and incon- gruent trials. Another condition that tested ‘no-go’ responses indicated no difference between groups. Impor- tantly, greater activity in the bilingual network, including areas identified in the meta-analysis [91], was related to smaller RT costs for incongruent trials. There are two implications of these results. First, bilingualism alters functional neural network at the response-selection level (congruent and incongruent trials), but not at the motor execution level (response inhibition no-go trials), a pattern consistent with previous results for both adults [102] and children [75,103]. Second, bilinguals showed a brain- behavior correlation when suppressing interference from conflicting flankers, replicating a previous study using magnetoencephalography (MEG) [104].

Box 1. Bilingualism in infancy

Research with infants being raised in bilingual homes has produced

dramatic evidence for very early effects of bilingualism and

challenges some standard explanations for the mechanism under-

lying these effects. It has long been known that children being raised

with two languages do not confuse the languages when learning to

speak, even though they may borrow from one when speaking the

other [127]. It is also well known that monolingual infants lose the

ability to make phonetic discriminations not present in their

language by approximately 10 months old, whereas bilingual

infants continue to distinguish between phonetic categories rele-

vant to all languages. Thus, it is not surprising that bilingual infants

can differentiate between their two languages essentially from birth

[128]. What is surprising, however, is the extension of this

discrimination to non-acoustic properties of language. Weikum

and colleagues [129] showed silent video clips to 8-month-old

infants who were being raised in homes that were either mono-

lingual English or English–French bilingual. Using a habituation

paradigm, the speaker switched languages after habituation and the

researchers measured whether or not infants regained interest. The

results showed renewed attention among the bilingual but not the

monolingual infants. To determine whether the bilingual infants had

learned about the facial structures that accompany each language or

something more general, the same materials were presented to

monolingual Spanish (or Catalan) infants and bilingual Spanish–

Catalan infants [130]. Again, only the bilingual infants noticed the

change in language, even though the children in this study had no

experience with either language. The authors concluded that

bilingualism enhances general perceptual attentiveness through

the experience of attending to two sets of visual cues.

This enhanced perceptual attentiveness may help explain the

results of a study in which 7-month-old monolingual and bilingual

infants learned a head-turn response to a cue to obtain a visual

reward and then had to replace that with a competing response for

the same reward [131]. Again, only the bilingual infants could learn

the new response. Even before children have productive language

ability, the experience of building two distinct representational

systems endows them with greater perceptual and attentional

resources than their monolingual peers. In light of such evidence

for bilingual advantages in the first year of life, explanations for the

mechanism responsible for the advantages found later may need to

be reconsidered to include a role for such perceptual processes.

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Although bilingualism is a language experience, man- aging attention to two languages imposes demands on the cognitive system that require brain regions not typically used for language processing. From studies of bilingual language switching and non-linguistic cognitive control, and from the meta-analysis cited earlier, it seems likely that the neural locus of cognitive control in bilinguals lies in bilateral frontal regions. In order to facilitate informa- tion transfer between the hemispheres, it is also possible that prolonged bilingual experience alters anatomical structures in addition to cortical functional networks. Cor- tical activity assessed by fMRI is limited to blood oxygen- ation level-dependent (BOLD) signal in the grey matter. However, when investigating domain-general neural changes (cognitive control) in response to domain-specific experience (bilingualism), it is important to use methods that allow not only the identification of functional net- works but also their underlying anatomical structures [105,106].

There is some evidence for the plasticity of cortical grey matter in response to bilingualism. Mechelli et al. [107] reported higher grey matter density in left inferior parietal regions in a group of Italian–English bilinguals relative to English monolinguals. Strikingly, proficiency in English, the second language, correlated positively with grey mat- ter density in this region. A recent study has extended brain plasticity to white matter. Luk, Bialystok, Craik and Grady [108] (Figure 1) used diffusion tensor imaging (DTI) and fMRI to measure white matter integrity and resting- state functional connectivity in monolingual and bilingual older adults. The results showed higher white matter integrity in bilingual older adults, primarily in the corpus callosum connecting the two hemispheres but also extend- ing to bilateral superior longitudinal fasciculi, right inferi- or frontal-occipital fasciculus and uncinate fasciculus. Identifying a seed close to the white matter voxels showing a group difference, Luk et al. conducted a resting-state functional connectivity analysis and showed that while both monolinguals and bilinguals had correlating brain activity with contralateral regions at rest, bilinguals had increased anterior-posterior connectivity. This evidence suggests that bilingualism is associated with better main- tenance of white matter structures in the course of normal aging [109]. Similar DTI results have also been recently reported in bilingual children around the left inferior frontal-occipital fasciculus [110].

The nature of the bilingual advantage Why might bilingualism be associated with an advantage in attentional control? The need to manage two jointly activated languages apparently leads to an enhancement of frontal-posterior attentional control mechanisms with the consequence that other types of cognitive control are also enhanced. Inhibitory control was suggested as the relevant mechanism in early studies [40,57] and continues to be endorsed by some researchers [47,111]. One problem with this account, however, is the recurrent finding of a bilingual advantage in congruent trials (for which there is no conflict) as well as incongruent trials [40,71]. Minimally, therefore, inhibition alone is insufficient to explain bilin- gual processing differences. The inhibition view is also

challenged by evidence from preverbal infants who dem- onstrate early effects of bilingualism but for whom lan- guage inhibition is not a plausible explanation (Box 1).

An alternative to inhibition is to consider the demands imposed by a mixed set of congruent and incongruent trials: there is always some probability that the next display may be an incongruent trial. Thus, even on con- gruent trials the display must be evaluated before the participant commits to a response. Congruent responses will typically be faster than incongruent responses, but individuals with superior attentional control processes (e.g. bilinguals) will be able to carry out such evaluative decisions more rapidly and effectively. Therefore, a differ- ent account of the bilingual advantage is in terms of conflict monitoring [39,81,82]. Evidence supporting this view comes from situations in which monitoring demands are low – if the majority of trials are of one type only [80,81], the potentially misleading information (spatial position in the Simon task, flanker items in the flanker paradigm) can be treated as a valid cue, even if the participant must respond in the direction opposite to that indicated by the cue. In such low-monitoring conditions the bilingual ad- vantage is typically not found. More generally, Hernández,

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Costa, and Humphreys [112] argue for a bilingual advan- tage in the deployment of attention, enabling them to resist ‘capture’ by irrelevant information; such differences in attentional control may be the consequence of superior conflict monitoring. Conflict monitoring and inhibition are not mutually exclusive: although monitoring is consis- tent with evidence that pure blocks of congruent trials are performed equivalently by monolinguals and bilinguals [102,113], an inhibition account is still required to explain evidence that pure blocks of incongruent trials are some- times performed faster by bilinguals, notably by older adults for whom the task is more effortful [102].

Another problem with a pure inhibition account is that bilingual advantages are only found with some types of inhibition. The relevant distinction is captured by the contrast between the concepts of ‘response inhibition’ and ‘interference suppression’ [75,114]. In response inhi- bition, a univalent stimulus is associated with a prepotent response that must be overruled, such as say ‘day’ to a picture of night or press ‘left’ when the arrow points right. Bilinguals typically show no advantage in these situations [75,103]. In interference suppression, a bivalent stimulus contains two cues, each associated with a different re- sponse, such as the word ‘red’ written in blue ink, so attention must be selectively focused on the relevant cue. Bilinguals typically outperform monolinguals on these tasks [21]. The hallmark of univalent response inhibition tasks is that the correct response can be pre-programmed before the cuing stimulus appears (e.g. ‘if sun appears I’ll say ‘night’; ‘if the arrow points right I’ll respond left’). On bivalent tasks, in contrast, the nature of the interfering information is not revealed until the display appears; for example, in the Simon task the participant prepares to respond on the left if the stimulus is green, but cannot prepare to deal with possible competing information until the display is shown. Bilinguals are more efficient at dealing with this online interference, in much the same way as the picture of a horse presented to a French/English bilingual would evoke both ‘horse’ and ‘cheval’, one of which must be suppressed. In a sense, the bilingual must constantly maintain the set of ‘respond in one language, suppress the other language’ whenever the possibility of two languages exists (cf. global inhibition). Further, this set maintenance must coexist with processing the stimuli and responses of the language currently utilized in a fluent and appropriate manner (cf. local inhibition). Thus, lan- guage use for bilinguals involves interference suppression, and the online monitoring required in both non-verbal task switching and language selection is similar.

The suggestion that bilinguals are particularly adept at maintaining the appropriate one of two (or more) relevant task goals or attentional sets in working memory has much in common with the notion of selection of wanted stimuli as opposed to inhibition of unwanted ones. The net effect is the same, but by this view the suppression of potentially interfering information is essentially a consequence of active selection of the relevant information, rather than a primary mechanism of direct inhibition. This view is consistent with that proposed by Colzato and colleagues [77], who concluded that the bilingual advantage is not due to the constant exercise of inhibition, but that learning to

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keep two languages separate leads to an improvement in selecting goal-relevant information from goal-irrelevant information.

The sum of the evidence places the bilingual advantage beyond the explanatory power of a single process, a simple neural network, or a single executive control component. Instead, the ongoing experience of monitoring two lan- guages, in conjunction with the need to monitor context, speaker, and other environmental cues while inhibiting attention to the currently unused but active language modifies how the mind and brain engage in ordinary conversation for bilinguals. The more effortful any of these components become, the more likely it is for bilingual advantages to emerge on non-verbal tasks. However, the impact of this modification may be seen most clearly on tasks that bear the closest resemblance to bilingual lan- guage use, such as task switching. In this case, it is easy to see how the task of attending to the shape of a stimulus instead of its color resembles the task of retrieving the name for an object in French instead of in English. Not surprisingly, these tasks are typically performed better by bilinguals than by monolinguals, although the details of those performances are not yet well understood: some studies report bilingual advantages on mixing costs indi- cating set shifting [82,102], whereas others report the advantage in local switch costs indicating response switch- ing [76,115]. More generally, it is important to point out that bilingual advantages are not always found, even on tasks for which such performance differences would be expected. Some of the conditions that support the appear- ance of a bilingual advantage have been discussed, such as the need for monitoring and difficulty of the conditions, but others are still unknown. Another factor in determining performance outcomes is probably the nature or degree of bilingualism in the participants (Box 2). More details about the specific tasks and precise language histories of the bilingual participants may resolve these differences.

Bilingualism and dementia The finding that bilingualism enhances cognitive control raises the possibility that lifelong bilingualism protects against age-related cognitive decline, and may even post- pone the onset of symptoms of dementia. In this case, bilingualism may be one of the environmental factors that contribute to cognitive reserve or brain reserve [116]. Cognitive reserve is the idea that engagement in stimu- lating physical or mental activity can act to maintain cognitive functioning in healthy aging and postpone the onset of symptoms in those suffering from dementia. These factors include education, occupational status, higher socio-economic class, and the continuing involve- ment in physical, intellectual and social activities [117– 119]. If bilingualism contributes to cognitive reserve, then bilinguals should maintain higher levels of cognitive func- tioning and cope better with symptoms of dementia than monolinguals who are otherwise equivalent.

To test this idea, Bialystok, Craik, and Freedman [120] examined the hospital records of monolingual and bilin- gual patients who had been diagnosed with various types of dementia. In spite of being equivalent on a variety of cognitive and other factors, the bilinguals experienced

Box 2. How bilingual?

Bilingualism is not a categorical experience but experimental

research designs require it be treated as such – participants are

monolingual or bilingual and differences in performance are assessed

for members of the two groups. However, individuals can never be

perfectly monolingual or bilingual: even the most monolingual

people have had some experience with another language, for

example as a school subject or a travel necessity, and all bilinguals

have preferred languages or preferred contexts for each. These

gradations raise three questions about the research results.

The first question is the possibility of a cumulative benefit for

multiple languages. If managing two languages enhances cognitive

control processes, then does further enhancement accrue from the

management of three or more languages, as explicitly proposed by

Diamond [132]? Research by Chertkow et al. [119] on Alzheimer’s

disease and Kavé et al. [123] on normal aging showed better

outcomes for multilinguals than for bilinguals, but there may be

significant differences between multilinguals and bilinguals that do

not exist between bilinguals and monolinguals. As we have

suggested, bilinguals are typically not pre-selected for talent or

interest but multilinguals may often be individuals with high ability

and motivation to learn other languages, factors which may impact

as well on cognitive performance.

The second question is the degree of bilingualism required for

these benefits to emerge. If bilingualism is protective against some

forms of dementia, then middle-aged people will want to know

whether it is too late to learn another language, or whether their

high-school French will count towards cognitive reserve. A related

question concerns the age of acquisition of a second language: is

earlier better? The best answer at present is that early age of

acquisition, overall fluency, frequency of use, levels of literacy and

grammatical accuracy all contribute to the bilingual advantage, with

no single factor being decisive [133] (Gigi Luk, PhD thesis, York

University, Canada, 2008). Increasing bilingualism leads to increas-

ing modification of cognitive outcomes.

Finally, if the benefits of bilingualism are at least partly explained

by the joint activation of two languages, does the similarity of the

two languages matter? Does Spanish–English bilingualism require

more (or less?) attentional control to maintain separation than say

Chinese–English bilingualism? In a study with children who spoke

English plus one of French, Spanish, or Chinese, there was no effect

of the type of bilingualism, and all bilingual children outperformed

monolingual children on tests of executive control [134].

Box 3. Outstanding questions

� Nature of the bilingual advantage: what are the limits and boundary conditions for the bilingual advantage and why are

bilingual advantages not always found? What is the role of the

standard components of executive control – inhibition, shifting,

and working memory – in bilingual differences in processing? Do

these relations change over the lifespan?

� Cognitive reserve: is the bilingual protection against cognitive decline similar to other types of cognitive reserve in terms of

mechanism and neural correlates?

� Brain correlates: what changes occur in the frontal lobes? Are there effects on other brain regions? What is the mechanism for

these experience-dependent changes in frontal networks?

� Psychopathology: what are the neural correlates of the protective effects for patients with dementia? Does bilingualism have

differential effects on various types of dementia?

Review Trends in Cognitive Sciences April 2012, Vol. 16, No. 4

onset symptoms and were diagnosed approximately 3–4 years later than the monolinguals. Specifically, monolin- gual patients were diagnosed on average at age 75.4 years and bilinguals at age 78.6. A replication from a new set of patients all diagnosed with probable Alzheimer’s disease (AD) [121] confirmed the results.

Three questions about these results are their reliability, validity, and causality. For reliability, several studies have replicated these findings. Chertkow et al. [122] reported partial support for the original results and showed that multilinguals were diagnosed with AD later than compa- rable monolinguals, although a more limited effect was found when monolinguals were compared with bilinguals. A similar positive relationship between multilingualism and high-level cognitive functioning was reported by Kavé et al. [123] in a study of elderly Israelis. Gollan et al. [124] reported a study with Spanish–English bilinguals who had been diagnosed with probable AD and found that a higher degree of bilingualism was associated with later age of onset and diagnosis, although only in the less-educated patients. (See Box 3 for further outstanding questions.)

Second, validity requires demonstrating the specific relation between the predictor and outcome variables.

Previously, socioeconomic status, cultural differences and immigration status have been suggested as contribu- tors to or even causes of the bilingual advantage. However, in both Toronto studies, educational level and occupational status favored the monolingual group and immigration status was ruled out as a contributing factor.

Third, regarding cause and effect, is it possible that people with ‘good brains’ are both resistant to dementia and also more likely to learn a second language? This is unlikely: most people do not become bilingual because they are bright or have a flair for learning languages, but rather out of necessity. Supporting this interpretation, a recent study showed that in a sample of monolingual and bilin- gual AD patients matched on age, cognitive level, and other factors, CT scans showed more AD pathology in the brains of the bilinguals, consistent with the idea that they are better able to cope with the disease and can function longer without showing symptoms [125].

Concluding remarks In the first study reporting the surprising outcome of an advantage in cognitive and linguistic performance by bi- lingual children, Peal and Lambert concluded: ‘Intellectu- ally [the bilingual child’s] experience with two language systems seems to have left him with a mental flexibility, a superiority in concept formation, a more diversified set of mental abilities’ ([9], p. 20). Peal and Lambert did not explain what they meant by ‘mental flexibility’ but the description works well to describe the data accumulated in the 50 years since their original study. Bilinguals do sometimes have an advantage in inhibition, but they also have an advantage in selection; bilinguals do sometimes have an advantage in switching, but they also have an advantage in sustaining attention; and bilinguals do some- times have an advantage in working memory, but they also have an advantage in representation and retrieval. To- gether, this pattern sounds like ‘mental flexibility’, the ability to adapt to ongoing changes and process informa- tion efficiently and adaptively.

It should not be surprising that intense and sustained experience leaves its mark on our minds and brains – the functional connections that come from practice are surely changed by massive experience, and the structural regions that are recruited for specific activities undoubtedly change as well through use. These responses to experience

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are precisely what we mean by neuroplasticity. Yet, in the case of bilingualism, the assumption has long been that any such effects would be deeply negative: as one influen- tial educational researcher commented in 1926, ‘This might be considered evidence that the use of a foreign language in the home is one of the chief factors in produc- ing mental retardation as measured by intelligence tests’ ([126], p. 393). Almost a century later, and in the face of substantial evidence to the contrary, there remains resis- tance to the idea that bilingualism can enhance aspects of cognitive function. Educational and clinical practitioners routinely advise parents to ‘simplify’ their children’s lin- guistic environment when there are signs of academic struggle, and language professionals prescribe optimal timetables (and methods) for introducing languages to children to minimize the inevitable confusion. But such views are based on fear and anecdote – the weight of scientific evidence supports the promise of ‘mental flexibil- ity’. There is still much we do not know about the effect of bilingualism on the mind, the neural correlates of those effects, and the causal components of the experience that lead to them. But it is too late to turn back: it is now clear that the bilingual mind has been uniquely shaped by experience.

Acknowledgments Preparation of this manuscript was supported by grant R01HD052523 from the US National Institutes of Health and grant A2559 from the Natural Sciences and Engineering Research Council of Canada to E.B.; grant A8261 from the Natural Sciences and Engineering Research Council of Canada to F.I.M.C.; and grant MOP57842 from the Canadian Institutes of Health Research to E.B. and F.I.M.C. We thank Steven Lovasz for his assistance in preparing the manuscript.

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Acquired Language Disorders in Bilinguals

Authors: *Elisa Cargnelutti,1 Barbara Tomasino,1 Franco Fabbro2,3

1. Scientific Institute, IRCCS E. Medea, Dipartimento/Unità Operativa Pasian di Prato, Udine, Italy

2. Cognitive Neuroscience Laboratory, DILL, University of Udine, Italy 3. PERCRO Perceptual Robotics Laboratory, Scuola Superiore Sant’Anna, Pisa, Italy *Correspondence to [email protected]

Disclosure: The authors have declared no conflicts of interest.

Received: 16.04.19

Accepted: 18.06.19

Keywords: Aphasia, bilingual, language disorders, language impairment.

Citation: EMJ Neurol. 2019;7[1]:101-109.

Abstract

The literature reports an increased number of aphasias involving bilingual people. Dealing with bilingual aphasia requires particular attention from the diagnostic to the therapeutic phase. In this review, the authors describe the possible impairment patterns, which could be different between the two languages and be characterised by specific deficits and sometimes unexpected profiles. The role of some crucial factors in determining the observed deficits and impairment patterns is illustrated, for instance age of appropriation and proficiency. An early versus late language appropriation recruits different brain processes and hence different brain structures. In general, a greater vulnerability is observed for the late-learned languages, although a high proficiency or use and exposure appear to prevent language impairment even in the case of late appropriation. The authors also discussed the role of other intervening factors, such as emotional–motivational aspects, which could explain unusual profiles. Furthermore, language deficits specific to bilingualism, such as pathological mixing and switching and translation problems were described. In this respect, the authors underlined the fundamental involvement of cognitive control mechanisms and of the brain structures associated with this. Lastly, the clinical practice issues in bilingual aphasia were outlined, underlining the need for a careful diagnosis. This should take into account the patient’s language history in order to avoid biased assessments and instead promote the setup of effective intervention programmes.

INTRODUCTION

The cases of bilingual aphasia are increasing worldwide, as they also reflect the globally increasing number of individuals speaking more than two languages (representing more than half of the population),1,2 who are referred to as bilinguals, irrespective of the number of known languages. Bilinguals differentiate one another

under multiple aspects and their clinical language profiles may differ. In this review, the authors provide an overview of the different bilingual aphasia profiles and the factors associated with these different conditions, providing hints for their understanding and treatment.

In relation to the different patterns of language impairment or recovery, Paradis3 proposed, in

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1977, the first structured classification: a) parallel impairment, in which the languages are similarly compromised; b) differential impairment, in which one language is more affected than the other; c) selective impairment, in which only one language is affected and the other is spared; d) blended or mixed impairment, in which there is interference between the languages and the patient cannot keep them separated; e) antagonistic, in which improvement in one language is associated with an increased impairment in the other and vice versa; and f) successive recovery, characterised by improvement in one language taking place only after the complete recovery of the other.

These impairment patterns reflect the interplay between many factors. These include first the clinical parameters that shape aphasia in monolinguals as well, such as lesion volume or patients’ age, but, crucially, also the patients’ language background. To this regard, the age at which the patients were exposed to the non- native or second language (L2) is also crucial.4,5 Age of acquisition or appropriation (AoA) is critical as it influences the way the language is represented in the brain. Neuroimaging studies in healthy bilinguals usually take the age of 6 as the cut-off to differently investigate the brain networks associated with an early versus late L2 appropriation, because around this age crucial developmental changes occur in the brain and in the learning mechanisms. Indeed, up to this age, language appropriation takes place in the form of acquisition, meaning an almost unconscious process supported by implicit mechanisms. Otherwise, late appropriation is defined in terms of learning, which instead relies on explicit processes.6-8

According to authors such as Paradis and Ullman,6-9 the role of AoA differs based on the considered language structural domain. It is particularly crucial for morpho-syntax and phonology/articulation. Internalisation of the related processes and, hence, native-like proficiency can only be achieved with early acquisition, relying on implicit mechanisms. On the other hand, lexical knowledge depends more on the degree of language use and exposure, as it is supported by explicit memory. Besides AoA, other factors also influence language mastery and related brain representation, with the chief role of proficiency.10 The following paragraphs

illustrate these main factors and relate them to the impairment patterns.

PATTERNS OF LANGUAGE IMPAIRMENT IN BILINGUAL APHASIA

Cases of either parallel or differential impairment are reported in many studies as the sole conditions, indicating their higher incidence with respect to the other impairment patterns. For instance, Fabbro described 20 bilinguals (AoA up to 7) with left-hemisphere damage, of whom 65% manifested parallel impairment and the remaining differential impairment. In these, either the native, first language L1 (15%), or non-native, L2 (20%), were affected the most.11 According to Paradis, the overall most frequent condition is parallel impairment, although it is underrepresented in literature, probably because it appears less appealing and therefore less worthy to be reported.6,7

Parallel impairment is frequently observed between non-native languages (for patients knowing more than two languages) when these had similar AoA, in particular when they shared the same learning modality (e.g., formal instruction).12 However, parallel impairment was also observed irrespective of AoA. For instance, Green et al.13 reported a parallel impairment between L1 and English, the L2, in patients having lived in the UK for many years, indicating the fundamental role of language use and exposure.13 The authors, however, attributed this condition to impaired control abilities, which is discussed further.

Concerning differential impairment, many patients follow either the so-called Ribot’s rule, postulating better preservation of L1,14 or the Pitres’ rule, according to which it is the most familiar language to be better preserved.15 In fact, although it is more intuitive to hypothesise greater resistance to damage for the language learned first, in many cases L1 was instead the most affected. This occurred, for instance, when the patients had a premorbid high level of L2 proficiency and frequency of use, although a recent systematic review seemed to restrict this possibility to early bilinguals.16

The patient described by Samar and Akbari17 had more preserved L2, which she learned at school, then studied at university and taught there

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as a teacher for 18 years. In this case, the high and deep knowledge of the language together with its constant use reduced the impairment severity. In healthy adults, the language networks appeared highly similar between L1 and L2 when proficiency is high.10 The learning method, represented by formal instruction, also had a possibly relevant role. In fact, as long as the brain lesion spares the explicit learning system and therefore the consciously learned meta-linguistic skills, formal knowledge, which relies on them, can potentially promote language recovery. This view is supported by the cases of an apparently paradoxical profile in which the patients were impaired in their native language but retained the use of an only-formally learned language, including the dead languages, such as Latin.18

Nevertheless, main exposure alone can not assure the language preservation. Impairment can indeed occur in cases of L2 learning that took place recently19 or in adulthood,20 when the brain is less prone to remodelling and language brain representation, therefore results can be less sound, hence more vulnerable to damage.

All the aforementioned language background factors indeed shape the language brain representation. Tangible information about the bilingual patients’ brain networks mainly comes from intraoperative stimulation studies. In a large- cohort study, Roux and Trémoulet21 observed that only two patients displayed solely common stimulation sites between the two languages, whereas the majority of them had both common and language-specific sites. Interestingly, language-specific sites were observed even in early bilinguals and, secondly, no additional cortical sites were found for the less-proficient language. There were similar results from a subsequent study on late but proficient bilingual patients, which further reported ‘L2-restricted zones’ in the perisylvian cortex, i.e., sites associated exclusively with L1.22 Although these findings were limited to the scouting of the affected region and its surroundings, they show that even close brain sites may be dedicated to different languages and that sometimes neither AoA nor proficiency can predict the extent of different representation between the two languages.

The depicted language brain representation leads us to suppose that a brain lesion, unless it is small and circumscribed, hardly affects one language while completely sparing the other. Nevertheless, a few cases of selective language impairment have been reported. This phenomenon was described in patients with epilepsy, with a selective postictal temporary loss of either L123,24 or L2.25 This specific type of impairment may hence have a neurofunctional rather than a neuroanatomical substrate. Changes in the normal brain electrical activity may temporarily inhibit the circuits associated with a specific language, which is recovered when the normal brain functioning is restored. In this vein, selective recovery might also result from impairment in control functions, which is illustrated in the following chapter.

The reversible inhibition of one language characterises another apparently odd condition, naming the alternating antagonism. This phenomenon is characterised by phases in which only one language seems to be accessible, whereas the other is apparently lost, and usually takes place in the immediate post-event period.26 This confirms the hypothesis that the impaired language is not lost, but inhibited, and that when this inhibition resolves, either spontaneously or throughout rehabilitation programmes, the language may recover.

Alternating antagonism is likely to take place when there is an underlying deficit in the regulation processes, which caused competition even between structurally distant languages, such as Farsi and German, as seen in the patient described by Nilipour and Ashayeri.27 The patient also manifested a successive recovery, with English (L3) recovering only after the complete recovery of the other two languages.

ROLE OF COGNITIVE CONTROL IN BILINGUAL APHASIA

Bilingualism indeed entails the need to coordinate language use to activate the proper language according to the context, while suppressing the irrelevant. This entails the constant recruitment of cognitive control functions and a certain degree of cognitive flexibility to properly shift from one language to the other.28 This could be the reason of the cognitive advantage some studies

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observed in bilinguals with respect to monolinguals, even in presence of aphasia.29

According to the neural convergence hypothesis,30 as bilinguals become more familiar with the new language, its brain representation converges with that of the native language. In this perspective, differences rather rely on the diverse recruitment of the cognitive control resources. Moreover, Radman et al.31 observed language improvement following stroke to be associated with increased connectivity between language areas and those devoted to cognitive control.31 However, they noticed this phenomenon was restricted to the language that improved the most, therefore suggesting that, at least in some cases (e.g., different AoA or proficiency), differences in the neural representation between the languages can actually be present.

Control deficits were observed in both parallel13,32 and differential or selective language impairment.33 Recently, many studies aimed to understand whether possible cognitive control deficits in bilingual aphasia. Some studies seem to suggest a language-specific control deficit,32 although problems in general control were also observed, and the interplay between other intervening factors, such as task complexity or lesion site were proposed to modulate the relation between language and control deficits.13,34

In their recent review on the neuroimaging of language control, Abutalebi and Green28 recapitulated their previous studies on the topic by illustrating the specific role of the brain structures associated with the language control network. These include both cortical (i.e., prefrontal cortex, dorsal anterior cingulate cortex/pre- supplementary motor area, and inferior parietal cortex, with the involvement of both hemispheres) and subcortical regions (i.e., left basal ganglia and thalamus and right cerebellum). These regions are deputed to specific functions within the language control process and lesions at their level might cause different control deficits.

Among these regions, extensive literature has highlighted the crucial role of the basal ganglia, and particularly the left (head of the) caudate and putamen, which are involved in appropriate language selection. Aglioti and Fabbro35,36 reported the case of a woman who lost her ability to speak her first language (an Italian dialect), but surprisingly began to speak Italian, which she had learned at school but rarely spoke throughout her life.35,36 She also began to speak with a strong German accent, a phenomenon known as foreign accent syndrome and described even in monolingual patients (Figure 1).

A z=36mm T value T valuez=44mmB

Figure 1: Foreign accent syndrome.

Foreign accent syndrome is a rare acquired motor speech variation, which has been reported in about 60 cases in literature.37 Patients suddenly exhibit a seemingly 'strange' accent and are perceived as having a foreign accent by listeners of the same speech community. Tomasino et al.38 reported a tumoral patient developing foreign accent syndrome following a small and circumscribed lesion in the left precentral gyrus. The patient, an Italian native speaker, developed altered speech rhythm and melody. During pronunciation of words and pseudowords in fMRI tasks, the patient showed a hyperactivation, compared to the control group, in areas around the pre/postcentral gyrus corresponding to those involved in phonation (i.e., larynx motor area). The fMRI cluster related to mouth (A) and tongue (B) movements located behind the patient's lesion (indicated by the red circle).

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This is a case of paradoxical use of one language and can be explained in light of the lesion location, which affected the left basal ganglia,39 and also stresses the role of the subcortical structures in implicit memory processes, which normally support the early acquired languages.

For the role the basal ganglia plays in implicit memory processes, a lesion at this level is likely to predominantly affect the mopho- syntactic processes. This was reported even for late-learned languages of high proficiency, for which even these linguistic processes could have become automated.40 This result indicates the crucial role proficiency may have in promoting language representation reshaping throughout life.

An illustrative case of the association between lesion site and impaired language was described by Moretti et al.41 The patient manifested impairment in the native language following an infarct in the left caudate nucleus and then, when a lesion affected the left frontotemporal cortex, she developed deficits in her late-learned L2. This supports the predominant cortical representation of languages learned through explicit processes, although an opposite trend was also described.42

OTHER CLINICALLY RELEVANT FACTORS

Recovery patterns may also be modulated by factors other than AoA, proficiency, and cognitive control deficits (see Figure 2 for an overview). Bilinguals learning a new distant language try to adopt the same L1 processes, but when these turn out to be unsuitable, they need to develop new processes (assimilation-accommodation processes).43 Evidence is however lacking regarding the possibly greater impairment in L2 when structurally distant from L1.16

Recorded difficulties reflect the cognitive demands required to process a given language, for instance when reading a transparent versus opaque language. This point is tricky as these differences might bias the diagnosis between the languages,44 and therefore call for a language assessment respectful of language complexity.

Other factors contributing to the definition of a given impairment pattern include the language spoken in the environment, namely in the hospital, in the period immediately following the clinical event. This factor can also be relevant from the rehabilitation viewpoint, as lower-than- expected improvements in the treated language were attributed to the fact that the patient was constantly exposed to another language outside the rehabilitation setting.45

Premorbid parameters (language history)

AoA Language features Postmorbid proficiency

Lesion site and severity

Premorbid proficiency

Languistic distance Postmorbid use/

exposure

Postmorbid use/ exposure

Emotional-motiva- tional factors

Patient's age

Learning method Cognitive control

problems

Rehabilitation

Postmorbid parametersClinical parameters Other factors

Figure 2: Overview of the factors contributing to the different language recovery patterns.

AoA: age of acquisition or appropriation.

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Finally, even the affective factors can assume a fundamental role. Emotionally relevant episodes may induce the release of the apparently lost language46 and the willingness to recover a given language may actually prompt its improvement.47

SPECIFIC LANGUAGE DEFICITS IN BILINGUAL APHASIA

Differently from monolinguals, bilingual patients may develop deficits characterising specifically the bilingual condition and concerning the reciprocal use of the two languages. These symptoms include mixing (i.e., recourse of words or other elements of one language during the use of the other), switching (e.g., shift from one language to the other), and problems in translation.

Frequently, these events arise from lesions in the mentioned areas involved in regulating the proper language use,48,49 with greater interference frequently observed between two structurally close languages.19,50 Fabbro et al.51 described the case of a patient with a glioma in the left prefrontal and cingulate cortices who involuntary switched to his native language, even talking to people he knew could not understand it, indicating the inability to inhibit the process.

Lesions in other areas were observed to pathologically induce or prevent language switching and include the inferior parietal lobe52 and the fronto-temporal cortex.53 Interestingly, switching was observed during direct electrostimulation of specific brain sites (Figure 3), including the white-matter tracts connecting control and language-specific brain areas.56

In some other cases, these phenomena reflect language impairment, as they occurred to compensate for anomia or other difficulties in the more impaired language.57,58 This can also be the case of translation deficits, which often reflect the general impairment in a specific language, with greater difficulty in translating from better preserved to more impaired languages than vice versa. Sometimes, this language deficit occurs selectively, despite spared ability in naming59 or in recognising translation equivalents across the languages.60 In other cases, in which naming abilities were impaired, translation processes were preserved, and further employed to recover word finding difficulties through translation from the preserved languages, therefore preventing switching.49

However, some patients were observed to paradoxically translate to the most affected language while unable to translate to the spared language,61 for instance when antagonistic recovery occurred.26 Sometimes, the patients instead manifest the compulsive tendency to

Figure 3: Switching from L2 to L1.

In neurosurgical patients, Penfield W and Roberts L54 largely documented language switching during electro- cortical stimulation mapping as an automatic mechanism that turns off one language when the other language is on. Tomasino et al.55 described involuntary language switching from L2 (Italian) to L1 (Serbian) evoked by electro- stimulation in the left superior temporal gyrus/supramarginal gyrus during awake brain surgery. The language switching site belonged to an fMRI cluster in the area Stp (in the planum temporale) which has a role in phonological processing and was found to activate for both L1 and L2 during language tasks. The language switching site (MN1 coordinaltes: x=-61, y=-30, z=18)

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translate from one language to the other, while not being able to prevent this automatic behaviour.39

ISSUES IN BILINGUAL APHASIA

Dealing with bilingual aphasia requires specific precautions from the diagnostic to the therapeutic phase. Firstly, for a proper diagnosis, it is fundamental to take into account the level of premorbid language proficiency, which was observed to be one of the most important factors in predicting the postmorbid level of deficit.62 Hence, it is fundamental to first thoroughly inspect the language history (e.g., AoA, proficiency, frequency, and context of use) by means of structured questionnaires.

Secondly, clinical assessment should ideally be performed in all the languages the patient knows, even though, especially for immigrated people, clinicians may not master the patient’s L1. When testing the different languages, it is also fundamental to take into account the structural differences between them. To this aim, Paradis and Libben developed the Bilingual Aphasia Test (BAT), now available in >70 languages, with items for each language matched in complexity and selected for their cultural adequacy.63 The battery is structured in three parts: the first inspecting the language history, the second making a comprehensive assessment of each language skills, and the last addressing specific language pairs, offering an understanding of which language was affected the most. A proper diagnosis is fundamental for setting the rehabilitation programme. Ideally, each impaired language should be treated. When this is not possible, therapists should train the language that could have more beneficial effects on the untreated language, therefore promoting cross- linguistic transfer. Although not univocally, many studies have observed that treatments focussing on the weaker language, meaning a non- native language64 or, in the case of comparable AoA, a lower-proficiency language65 are more likely to boost improvements in the untreated language.62,63 With regard to naming training, this trend can be explained in light of the revised hierarchical model by Kroll and Stewart,66 according to which L1 words are tightly linked to their correspondent meaning, whereas L2 word semantic access occurs via translation to L1. Consequently, semantic access after L2 training likely takes place by passing through the L1 lexicon, which recovers in turn. In the case

of difficulty in properly regulating the language use, rehabilitating general cognitive functions is recommended first.67

Gil and Goral,68 however, qualitatively observed beneficial transfer effects following treatment in each language, in spite of the structural distance between them (i.e., Russian and Hebrew, for which transfer was poor only in/for writing, which differs substantially between them). However, they tested the patient in the subacute phase, when spontaneous recovery was also taking place. The majority of the reported studies, however, took charge of the patients in the chronic phase and documented positive treatment effects as well. Language skill improvement and associated brain reorganisation were observed to occur just 10 days after intensive training, indicating the high brain plasticity potential even many months post-onset.69

According to Kiran et al.,70 all the parameters that have been described, such as AoA, language use, and proficiency before and after the clinical event, are relevant for the prediction of the recovery profile following treatment, although their interplay and the intervention of additional factors undermines an accurate prediction. In some instances, lack of transfer can be attributed to factors other than the treated language. These can include the choice of inappropriate rehabilitation strategies,71 the impossibility to practice the treated language outside the rehabilitation setting,45 the fact that the unimproved language had already reached its highest recovery level.72 Lastly, some partly unexpected improvements might be attributed to the willingness to recover a given language, highlighting the emotional valence the languages can take on.47

CONCLUSION

In conclusion, although it is difficult in clinical practice to concretely take account of the bilingual patients’ languages, some attempts should be made to achieve an accurate diagnosis and guarantee the most effective possible therapeutic intervention, as impairments in a given language can have relevant consequences for the patients’ life on social, affective, and working levels.

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