Abstract
Despite the large number of elderly bilinguals at risk for Alzheimer’s disease (AD) and dementia worldwide, significant questions remain about the relationship between speaking more than one language and later cognitive decline. Bilingualism may impact on cognitive and neural reserve, time of onset of dementia symptoms and neuropathology, and linguistic competency in dementia. This review indicates increased cognitive reserve from executive (monitoring, selecting, inhibiting) control of two languages and increased neural reserve involving left frontal and related areas for language control. Many, but not all, studies indicate a delay in dementia symptom onset but worse hippocampal and mesiotemporal atrophy among bilinguals versus monolinguals with AD. In contrast, bilinguals do worse on language measures, and bilinguals with AD or dementia have difficulty maintaining and monitoring their second language. Together, these studies suggest that early-acquired and proficient bilingualism increases reserve through frontal-predominant executive control, and these executive abilities compensate for early dementia symptoms, delaying their onset but not the neuropathology of their disease. Finally, as executive control decreases further with advancing dementia, there is increasing difficulty inhibiting the dominant first language and staying in the second language. These conclusions must be interpreted with caution, given the problems inherent in this type of research; however, they do recommend more work on the pre-dementia neuroprotective effects and the dementia-related language impairments of bilingualism.
INTRODUCTION
Bilingualism, or the use of two languages in everyday life, has unique implications for the large numbers of elderly persons throughout the world who are at risk for, or already have, Alzheimer’s disease (AD) and other dementias. Understanding this relationship involves clarifying how bilingualism affects dementia risk and, conversely, how dementia affects language among bilinguals. Given the absence of disease-modifying treatments for AD, the identification of modifiable, environmental factors such as bilingualism is an increasing focus of AD research [1]. If symptoms of dementia could be postponed through bilingualism, there could be major savings in both human costs and health economic considerations [2]. There is also a need for greater attention to the specific cognitive and linguistic consequences of bilingualism among patients who are already suffering from dementia [3–5].
In order to evaluate the relationship of bilingualism and dementia, this review looks at bilingualism in a broad context. First, there are implications of using more than one language on cognition and on brain structure and function, or cognitive and neural reserve, in normal individuals. Second, this review includes a critical re-examination of the impact of bilingualism on the onset of both dementia symptoms and the neuropathology of these disorders. This is worth re-examining because of conflicting meta-analyses of the literature [6–8], including questions about choice of studies and other issues [9, 10]. Third, it evaluates the question of how bilingualism affects linguistic competence among those who already have a dementing illness. The current literature is problematic because of potential inaccuracies in establishing bilingualism, including age of acquisition and proficiency, and confounding variables such as education and acculturalization. Nevertheless, tentative conclusions can be drawn on this important topic that can guide future research studies (See Table 1).
Significant Findings from Literature on Bilingualism and Dementia
COGNITIVE RESERVE AND NEURAL RESERVE
Cognitive reserve
Cognitive reserve involves the optimization of cognitive strategies and brain resources. Cognitive reserve posits that cognitive efficiency, capacity, or flexibility are altered by life experience regardless of quantitative brain measures [11, 12]. These life experiences include education, occupational attainment, engagement in leisure and social activities and, possibly, the regular use of two or more languages. In an important study of Scottish children born in 1936 and followed and retested in later life (the Lothian Birth Cohort), those who learned a second language after age 11 achieved better cognitive results independent of childhood intelligence, suggesting an effect of bilingualism on cognitive reserve [13]. Other investigators found that the number of languages spoken predicts cognitive performance in the oldest old, over and above contributions of age, gender, immigration status, and education [14]. In the presence of greater cognitive reserve established by higher education, there is a requirement for more pathology in AD, indicating optimal utilization of brain resources to cope with neuropathology [15]. Bilingualism may also function like education to increase cognitive reserve and protect against cognitive decline in the presence of the neuropathology of AD [16–19]. For example, in a population-based study in Luxembourg, investigators found that pervasive multilingualism could be a factor in the low prevalence estimates of cognitive complaints and dementia in adults over the age of 64 years [20].
The key to understanding how bilingualism affects cognitive reserve is the “Joint Activation Theory”, i.e., both languages are automatically, constantly, and often unconsciously active in monolingual contexts [18, 21]. The effect of bilingualism on cognitive reserve is through the optimization of language and executive control of two active representations that compete for selection [22]. The regular activation of two languages may increase cognitive reserve through training executive functions in the constant management of two simultaneously active languages, which leads to highly practiced cognitive control mechanisms in bilinguals relative to monolinguals [18, 24]. This neurocognitive language or “bilingual language control model” encompasses executive processes such as goal maintenance, conflict monitoring, interference suppression, and selective response inhibition [25, 26]. In other words, since both languages are activated when one is being used, bilinguals must continuously resolve competition for selection between lexical forms in the first and second languages via active inhibition of the non-target language [27, 28]. In addition to inhibition, bilinguals must monitor their environment to determine which language should be selected [29]; hence, bilingualism is constantly activating the executive control processes of monitoring, selecting, and inhibiting. Further evidence for this model comes from language switching studies showing greater costs in releasing from active inhibition of the dominant or first language (L1), as opposed to the less dominant or second language (L2) [30], and other investigators report that participants engaged in an L2 task have difficulty entirely suppressing activation or eliminating interference from their L1 [31].
These linguistic control tasks emphasized in bilinguals are the same executive control mechanisms used for nonlinguistic tasks, including attention and conflict monitoring, switching, interference suppression, and response inhibition [26]. This means that bilinguals may exhibit better general executive abilities relative to monolinguals [32]. Consistent with this view, bilinguals have performed better than monolinguals on the following executive tasks: digits backwards and the Trail Making Test-B [23], the Stroop task [33], the Erickson Flanker task [34], and the Simon Effect (stimulus-response location compatibility) [35–38]. Studies have shown that, compared to monolinguals, bilinguals have better attention control mechanisms for conflict resolution even in non-language contexts [39–41], the ability to switch between two tasks [42–44], resistance to irrelevant or competing stimuli and proactive interference [32, 45], inhibition of lexical competitors when retrieving words from semantic memory [46, 47], and greater processing speed when tasks require significant monitoring resources involved in executive control [48]. Other related tasks implicated as better in bilinguals versus monolinguals are the updating of information in working memory, the ability to reverse ambiguous figures, and performance on global-local processing [49]. Finally, it is important to note several studies that have failed to find an advantage for bilingual seniors during executive control tasks [50–52].
Neural reserve: Activation-functional studies
Beyond cognitive reserve, bilingualism may enhance neural reserve, or the activation, structures, and connections of the brain [53]. Functional magnetic resonance imaging (fMRI) analyses reveals that both monolinguals (in one language) and early proficient bilinguals (in each language) have increases in activation in classic language areas such as the left inferior frontal cortex (Brodmann’s area 45) [54]. Major differences in activation depend on age of acquisition and proficiency in L2 [55], with early acquisition (<6 years of age) and greater proficiency associated with similar left hemisphere activation as for L1, plus additional involvement of the right hemisphere among bilinguals [55–58]. In contrast, late bilinguals (>6 years) and those with less proficiency in L2 have more extensive lateralization and activation in the left hemisphere, without the right hemisphere involvement, compared to monolinguals [57–59]. Perani et al. (2003) found less extensive brain activation during a lexical retrieval task in earlier-acquired L2 [60]; whereas Vingerhoets et al. (2003) found greater cortical activation in later-acquired L2 [59]. In sum, despite some inconsistencies, it appears that a second language that is acquired early behaves much like L1, but a second language that is acquired late is more demanding, with greater neural activity and more widespread activations due to greater recruitment of left hemisphere areas associated with increased cognitive effort [61–63].
Bilingualism recruits left hemisphere frontal regions for both traditional language functions and for control of language interference, switching between languages, and language selection [64–67]. Depending on age of acquisition and proficiency, performing language tasks such as naming objects in L2 versus L1 requires more neural activity in the left inferior frontal lobe, especially in the left inferior frontal cortex (Brodmann area 45) [54, 68]. The left dorsolateral prefrontal cortex (DLPFC), left inferior and middle frontal gyri, and anterior cingulate cortex (ACC) are further implicated in language switching, in picture naming, and in selecting languages [68, 69], even in code switching during transcranial magnetic stimulation for depression [70]. The caudate nuclei, which mediate frontal-subcortical tracts, may be responsive to changes in language and monitoring and controlling the language in use, and the left caudate nucleus may be particularly implicated in code switching [69, 71]. In addition to left frontal regions, other areas involved in language control among bilinguals are the superior (right more than left) and middle temporal gyri (left more than right), the right precentral gyrus, midline pre-supplementary motor area, and the left parietal lobe, which participates in maintenance and implementation of task separations [69, 72–74].
If bilinguals learned L2 early or are proficient in that language, fMRI shows a pattern of increased efficiency with less need to activate language control mechanisms, and there may even be reduced frontal activity on nonverbal executive control tasks compared to monolinguals [75]. L2 proficiency, including the daily exposure to a second language with maintenance of language control mechanisms, may be the most important factor in the functional organization of bilingual language, and this could mitigate the typical effects of healthy aging [76]. Active L2 use drives cognitive and neural adaptations toward maximum efficacy [22]. Notably, the normally increased recruitment of frontal executive regions with aging is less pronounced and more efficient in bilinguals with increasing L2 proficiency [23, 77]. Early-acquired, proficient bilinguals also have increased functional connectivity between inferior frontal gyrus and regions of the brain supporting language control such as the salience and frontoparietal networks, between white matter regions mediating connectivity in nonverbal executive control tasks, and between right and left inferior frontal gyri [34, 78–81].
Neural reserve: Structural correlates
Compared with monolinguals, bilinguals generally show greater measures of gray matter in the left frontal language and language control areas [75, 82]. In particular, bilinguals have more cortical thickness in the left inferior frontal gyrus [82]. Among bilinguals, there is increased left and right ACC gray matter with better conflict monitoring and performance on the Erikson Flanker task [34, 83], and increased gray matter in the left inferior frontal gyrus is correlated with an increase in L2 proficiency in adults learning a second language [84]. Other areas which may be increased in bilinguals are the left anterior inferior temporal gyrus, temporal poles, and left Heschl’s gyrus [85, 86]; the left basal ganglia especially the putamen [87, 88]; and the left and right cerebellum [89]. There also appears to be increased gray matter density in left inferior parietal cortex (posterior supramarginal lobule and possibly angular gyrus) in early-acquired or proficient bilinguals relative to monolinguals [90–93]. Finally, bilinguals fail to show age-related decreased gray matter in the DLPFC, which occurs in monolinguals and is correlated with decreased executive performance [34].
Reports on white matter changes among bilinguals are less consistent than those for gray matter changes. Most investigators find greater frontal (DLPFC, ACC) lobe white matter among lifelong bilinguals compared to monolinguals [79]. With increased L2 experience among older bilinguals versus monolinguals, diffusion tensor imaging (DTI) studies indicate increased white matter integrity by increased fractional anisotropy in the corpus callosum, the inferior and superior longitudinal fasciculi, and other white matter tracts [75, 95]. Others find greater axial diffusivity, another DTI measure of white matter integrity, in the left superior longitudinal fasciculus of bilinguals compared to monolinguals [96]. Bilinguals also have greater white matter connectivity between left and right frontal cortex [94], and greater white matter volume in the frontal and temporal lobes [79]. In contrast, one study of older bilinguals versus comparable monolinguals reports lower fractional anisotropy values in inferior longitudinal fasciculi, inferior fronto-occipital fasciculus, fornix, and in areas of the corpus callosum [97], possibly consequent to the inclusion of patients at risk for early AD.
BILINGUALISM AND DEMENTIA ONSET
Delays onset
There are published reports from around the world indicating a protective effect of bilingualism against the clinical symptoms of dementia, delaying the onset by 4-5 years [18, 98–104]. This effect has been most evident when L2 is acquired early in life or if L2 is used proficiently [6, 106]. After adjusting for life expectancies, countries with large bilingual populations have reported lower incidence rates of dementia than more monolingual countries [107]. In a study from Canada, among 184 patients with dementia, 51% of whom were bilingual, the bilinguals showed symptoms of dementia 4 years later than monolinguals [18]. In a follow-up to this study with a new sample of 211 patients with probable AD, the bilingual (n = 102) patients were diagnosed 4.3 years later and reported the onset of symptoms 5.1 years later than the monolingual (n = 109) patients [98]. A Chinese investigation reported that Cantonese-Mandarin bilinguals had an older age at AD onset, and older age at the first clinic visit, than Cantonese or Mandarin monolinguals [99]. From India, other investigators compared the age of onset of first symptoms between bilingual (n = 390) and monolingual (n = 257) dementia patients and concluded that bilinguals developed clinical dementia 4.5 years later than monolinguals [100]. This group also reported a delay in post-stroke cognitive impairment and behavioral variant frontotemporal dementia, but not in other forms of frontotemporal lobar degeneration or progressive supranuclear palsy [101, 102]. Among 134 participants from Belgium with probable AD, 69 bilinguals experienced first symptoms (4.6 years) and diagnosis (4.8 years) significantly later after controlling for demographics [103]. Finally, investigators compared age at the time of receiving an AD diagnosis in bilingual Welsh-English speakers (n = 37) and monolingual English speakers (n = 49), and, although they did not find a significant difference in age at the time of diagnosis, the bilinguals were on average 3 years older than the monolinguals and significantly more cognitively impaired at the time of diagnosis [104]. These worldwide, but mostly retrospective, studies commonly evaluated symptom onset [10], and, despite criticism [8], appear to have significantly accounted for cultural and educational variables [9].
Important variables that deserve special attention include the presence of mild cognitive impairment (MCI), which may be precursor to clinical dementia, the level of education, and multilingualism (speaking three or more languages) compared to bilingualism. Among 74 MCI patients and 75 AD patients [108], the bilingual patients were several years older than comparable monolinguals at both age of symptom onset and date of first clinic visit. In other studies, those who spoke more than one language also had a lower risk for amnestic MCI and higher tissue density in temporal areas affected by AD [109–113]. Among 44 Spanish-English bilinguals, higher degrees of bilingualism were associated with increasingly later age-of-diagnosis (and age of onset of symptoms), but this appeared to be driven by participants with a low (<11 years) educational level [114]. Other studies, however, found differences between bilinguals and monolinguals in dementia onset despite clearly controlling for educational level, as well as occupational and immigrant status [100, 103]. In addition, at least on study found a small but significant protective effect for the use of three or more languages as compared to two languages [115].
Does not delay onset
Some prospective studies have not found a delay in dementia diagnosis. In the Einstein Aging Study (Bronx, NY) of aging and dementia (n = 1,779), there was no statistically-significant association between speaking some English as a second language and incident dementia or AD [116]. Among 1,067 participants in the Washington/Hamilton Heights Inwood Columbia Aging Project who were followed for up to 23 years, bilingualism was not independently associated with rates of cognitive decline or dementia conversion [117]. In the Sacramento Area Latino Study on Aging of 1789 community dwelling participants, the mean age of dementia diagnosis was not significantly different [118], but the study was confounded by significant effects of knowledge of L2 in monolinguals and by educational level [119]. These three U.S. studies had flaws in clearly determining knowledge of L2 among the bilinguals and/or the monolinguals. In a 1991 Canadian study, 1616 community-living older adults followed and assessed over five years later failed to show an association between being bilingual and having dementia on a limited screening measure [120]. Others failed to find a protective effect of bilingualism among 2520 Japanese-American men who self-reported using both spoken and written Japanese in mid-life [121]. The Australian Longitudinal Study of Ageing collected data on 2,087 older participants over 20 years [122] and found that bilingual and non-bilingual participants did not differ in decline in Mini-Mental State Examination scores. This last study also noted no significant bilingual-monolingual differences in baseline tests of executive function; however, the p value for these group baseline differences was 0.051 [122]. A final study of 514 community-dwelling people older than 70 years in Taiwan failed to find differences in dementia prevalence between multilingual (3 languages) and bilingual groups; however, the average age of the multilingual group was approximately two years older than that of the bilingual group [123]. These prospective studies have focused more on dementia incidence rates with issues of assessment of bilingualism, level of education, and the use of limited screening instruments [7, 120].
NEUROPATHOLOGY IN BILINGUAL DEMENTIA
Bilinguals with dementia may have more advanced temporal neuropathology than monolinguals with dementia at comparable clinical stages [10]. Bilingual patients with probable AD exhibit increased atrophy in temporal regions, specifically the radial width of the temporal horn and the temporal horn ratio relative to monolingual dementia patients matched on level of cognitive performance and years of education [124]. Others report similar or lower tissue density in medial temporal areas in multilingual patients with AD versus monolingual patients with AD despite comparable cognitive levels [113]. In contrast to increased temporal neuropathology, multilingual MCI and AD patients have thicker cortex than monolinguals in frontal and related areas for language and cognitive control, which correlated with performance on episodic memory tasks suggesting memory compensation via enhanced executive control abilities [113]. These findings support the presence of cognitive reserve from bilingualism as the bilinguals with AD withstand more temporal neuropathology while functioning at the same level in memory and cognition as monolinguals with AD [98, 124], possibly via increased frontal, frontostriatal, and frontoparietal executive control circuitry and the default mode network [77, 80]. Somewhat consistent with these structural changes, among 85 probable AD patients, cerebral hypometabolism was more extensive in the 45 bilinguals compared to the 40 monolinguals despite better memory and visuospatial skills [80]. L2 use in the 45 bilinguals correlated with increased metabolism in inferior and orbitofrontal regions and ACC despite decreased metabolism in several posterior brain regions [80]. Parenthetically, compared with monolinguals, early bilinguals have lower levels of t-tau in their cerebrospinal fluid, a biomarker of AD neuropathology [23, 125].
LANGUAGE COMPETENCY
Normals
Bilingualism results in changes in word production and in cross-language interference. Monolinguals generally outperform bilinguals on verbal naming [32], at least, in part, because bilinguals may use each language less frequently than their monolingual counterparts [126]. Bilingualism is associated with slower lexical retrieval of low frequency words and on picture naming in either language [18, 126–130], decreased word production especially in category or semantic fluency [33, 131–137], and more tip-of-the-tongue states in word production [138, 139]. Some studies also report lower performance in letter fluency in bilinguals than monolinguals [33, 133], but others have found similar performances [134, 136]. As word production becomes more effortful, bilinguals have increased fMRI activity in the DLPFC and the superior parietal lobule [68]. In older bilinguals, there is also an exacerbation of problems posed by the potential for cross-language interactions and interference [140]. Older bilinguals may struggle inhibiting L1 when speaking L2, resulting in increasing difficulty maintaining fluency in L2 [141]. Thus, these individuals may tend to retreat to their L1 dominant language, even those with a lifetime of bilingualism.
Dementia
The age-related verbal naming difficulty among normal bilinguals may be exacerbated due to dementia. The two languages are at least partially part of the same conceptual system and both are affected by AD-associated declines in semantic fluency and naming [142]. This may be evident in L1 early in disease or in the MCI-stage [143–148], hence, performance in the dominant language or L1 among bilinguals may better discriminate AD patients from healthy control subjects [146]. Bilinguals have more efficient compensation for early memory and cognitive impairments with more efficient frontal recruitment; however, as bilingual patients progress in dementia, the non-dominant language declines more steeply than the dominant language, and performance in L2 is particularly reduced [149]. A recent study of a bilingual patient with logopenic variant primary progressive aphasia, which is usually a variant of early-onset AD, showed lower performance in L2 than in L1, particularly in phonological processing, but parallel impairments in semantic processing [150]. Nevertheless, a few studies challenge the conclusion of worse L2 than L1 performance in dementia, reporting either similar or better linguistic changes in the two languages among bilinguals with AD or other dementias [151–154].
A prominent finding is the presence of increased cross-language difficulties, which is greatly exaggerated in those who develop dementia or AD [141, 156]. Bilingual dementia patients are particularly vulnerable to the effects of cross-language interaction, interference, and the need to maintain two languages in the face of mounting neuropathology, with reduced capacity to inhibit L1 and maintain fluency in L2 [141, 156]. Studies show that bilingual dementia patients have difficulty in language choice or selecting the appropriate language for a monolingual interlocutor and maintaining use of L2 while inhibiting L1 [141, 157]. There may be a lack of code-switching strategies and language mixing with advancing dementia as bilinguals code switch to their dominant L1 with excessive mixing in of L1 during monolingual L2 interactions [3, 158]. Further evidence of this is that, on reading aloud, bilingual AD patients, compared to bilingual controls have particular language intrusions from L1 when reading L2 [159]. With progressing dementia, this “reversion to L1”, their most conceptually-learned language may occur regardless of education, age of L2 acquisition, frequency of use, or baseline L2 fluency [156]. Although controversial, regression to L1 may even start prior to dementia onset [158].
LIMITATIONS OF THE RESEARCH
The research on bilingualism and dementia has been problematic and controversial for several reasons [160]. First, there are inconsistencies in the characterization of bilingualism across studies. Perhaps the most important is objectively determining level of proficiency in L2 [161], as language competency can vary greatly in the second language and can change depending on the interlocutor and the social situation. In addition, the speakers’ level of bilingualism is often measured using self-reports and is, thus, subjective, resulting in an inaccurate assessment of the individual’s language skills [162]. Second, there are different varieties and subtypes of bilinguals. These include simultaneous versus sequential bilinguals which usually corresponds to early versus late age of acquisition, productive versus receptive bilinguals, and balanced versus monolingual-dominant bilinguals. Third, there are prominent confounding variables such as education, context-dependent language use, immigrant status, family structure/support, and acculturation and nativity language [163, 164]. The degree of education and literacy may have a strong effect on performance and benefit from bilingualism [100, 166]. Bilingualism’s effects may also depend on whether they are in a home or familial context or in a formal or work context, as well as their immigration status [13, 167]. Finally, there is the issue of emotional, social, and cultural aspects of the two languages. The “meaning” of each language to the patient may vary considerably. There is data that L1 engages emotions more than a second language, with greater psychophysiological responses to emotional statements in L1 than in L2, whereas L2 increases psychological distance, with bilinguals more likely to endorse utilitarian outcomes in L2 [168, 169].
CONCLUSIONS
Despite the reservations on methodology, this review presents some tentative conclusions. Bilingualism increases cognitive reserve with improved executive control and increases neural reserve with improved left frontal and related (parietal, basal ganglia) areas and connections. This probably leads to delaying onset of dementia symptoms because of compensatory effects of frontal executive functions on memory and cognition, despite the accumulation of temporal lobe dementia pathology. The delay in symptoms but not disease may at least partially explain the difference between the delay reported in retrospective studies and the lack of delay in prospective studies. As the dementia advances and impacts on frontal language control, bilingual patients tend to asymmetrical language impairment characterized by greater reversion to L1 compared to L2 because of increasing costs of suppressing L1. This difficulty contributes to the abandonment of L2 and the retreat to a monolingual status. In sum, language use often reverts to the first learned language in bilingual patients.
These findings have clinical and research significance. Learning a second language may be an important mechanism for promoting cognitive and neural reserve and for delaying a functional decline from early dementia in later life through compensatory executive mechanisms. The constant usage of two or more languages and of bilingual/multilingual living contexts may promote cognitive and neural reserve. A few studies have even suggested that learning a second language in older age could build the kind of cognitive resiliency that retards the onset of dementia and promote neuronal white matter connections [170, 171]. Additionally, for clinicians and caregivers of bilingual dementia patients, it is crucial to understand the implications for early diagnosis, interventions, and effective communication with these patients as their dementia progresses. The dementia effects on bilingual language transcends effects on two individual languages as the dementia impacts on cross-language interference. The impaired fluency and regression to L1, with all its implications, from strictly linguistic to psychosocial, must be a consideration in the management of these patients. These areas, and others having to do with the relationship of bilingualism and dementia, deserve more research and investigation as the numbers of bilingual elderly patients at risk for, or already with dementia, continues to grow worldwide.
