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REVIEW ARTICLE
published: 03 December 2014
doi: 10.3389/fpsyg.2014.01401
Cognitive control, cognitive reserve, and memory in the
aging bilingual brain
Angela Grant 1,2 , Nancy A. Dennis 1,2 and Ping Li 1,2 *
1Department of Psychology, Pennsylvania State University, University Park, PA, USA
2Center for Brain, Behavior and Cognition, Pennsylvania State University, University Park, PA, USA
Edited by:
Hanako Yoshida, University of
Houston, USA
Reviewed by:
Marie-Josephe Tainturier, Bangor
University, UK
Arturo Hernandez, University of
Houston, USA
*Correspondence:
Ping Li, Department of Psychology,
Pennsylvania State University,
University Park, PA 16802-3106, USA
e-mail: pul8@psu.edu
In recent years bilingualism has been linked to both advantages in executive control
and positive impacts on aging. Such positive cognitive effects of bilingualism have been
attributed to the increased need for language control during bilingual processing and
increased cognitive reserve, respectively. However, a mechanistic explanation of how
bilingual experience contributes to cognitive reserve is still lacking. The current paper
proposes a new focus on bilingual memory as an avenue to explore the relationship
between executive control and cognitive reserve. We argue that this focus will enhance our
understanding of the functional and structural neural mechanisms underlying bilingualism-
induced cognitive effects. With this perspective we discuss and integrate recent cognitive
and neuroimaging work on bilingual advantage, and suggest an account that links cognitive
control, cognitive reserve, and brain reserve in bilingual aging and memory.
Keywords: aging, bilingualism, brain reserve, cognitive reserve, memory, neuroimaging
Bilingualism1research has recently generated much enthusiasm in
the study of the mind and brain (see Diamond, 2010;Bialystok,
2011). What has brought bilingualism to the center stage in cog-
nitive science? One key reason might be the perspective (and the
findings) that the bilingual’s experience with two or more lan-
guages conveys long-term cognitive benefits. Such benefits are
reflected in the fact that, compared to monolinguals, bilinguals
typically display enhanced cognitive control abilities, show more
mental flexibility, and can better handle tasks involving switching,
inhibition, and conflict monitoring (see Bialystok and Barac, 2013
for a review).
In the last decade a large number of studies have been devoted
to the study of the cognitive benefits of bilingualism. In these
studies, bilinguals generally show smaller effects of conflict (as
measured by reduced reaction time) across a variety of executive
control tasks, including the Attention Network Test (e.g., Costa
et al., 2008;Tao et al., 2011), the Simon task (e.g., Bialystok et al.,
2004), and the Stroop task (e.g., Coderre et al., 2013). Addition-
ally, these cognitive advantages have been shown to occur across
the lifespan in populations ranging from children (e.g., Bialystok
and Feng, 2008) to young adults (e.g., Bialystok et al., 2008)to
older adults (e.g., Bialystok et al., 2006). Furthermore, bilinguals,
compared with monolinguals, show delayed onset of age-related
cognitive decline in varying forms of dementia, such as Alzheimer’s
disease, by an impressive average of 4–4.5 years (Bialystok et al.,
2007; see also Alladi et al., 2013).
In this paper,we attempt to provide an account of the cognitive
effects (and advantages) due to bilingualism from a neurocog-
nitive perspective. Specifically, our goals are to (1) evaluate the
behavioral and neural bases of bilingual cognitive advantage, and
(2) suggest a mechanistic account for understanding the neural
1We use the terms “bilingualism” or “bilingual” here inclusively to refer to both
bilingual (two languages) and multilingual (more than two languages) situations.
basis of bilingual cognitive reserve in older adults by examining
the relationship between executive control, memory, and brain
reserve.
A number of researchers have suggested that the bilingual
experience in older adults may provide cognitive reserve, a pro-
tective mechanism that increases the brain’s ability to cope with
pathology (Bialystok et al., 2007;Luk et al., 2012;Abutalebi et al.,
2014a,b). In a review of cognitive reserve, Stern (2009) distin-
guished cognitive reserve from brain reserve. An earlier hypothesis
on brain reserve was the threshold hypothesis, according to which
there is a critical threshold past which the patient will show clin-
ically marked cognitive deficits (see Satz, 1993). Stern (2009,
p. 2016) defined brain reserve as “individual differences in the
brain itself allow some people to cope better than others with
brain pathology.” In this perspective, the mechanism underly-
ing brain reserve is thought to be quantitative: more neurons,
more synapses, better resistance to apoptosis, and so on, are used
in the individual to protect against age-related decline. Cogni-
tive reserve, in contrast, was defined by Stern (2009, p. 2016) as
“individual differences in how people process tasks allow some
to cope better than others with brain pathology.” Bialystok et al.
(2007) argue that bilingualism contributes to cognitive reserve
by improving the efficiency of executive control processing via
extensive, daily, experiences in handling two competing languages
(e.g., inhibiting the language not in use; see more discussion
below). Although these authors did not formally distinguish cog-
nitive reserve from brain reserve as did Stern (2009), their implicit
assumption was that cognitive reserve entails brain reserve (see
Luk et al., 2011).
To understand how bilingual experience provides the individ-
ual with cognitive reserve, we need to systematically examine the
cognition-brain-behavior relationship. On the one hand, there
must be a brain basis of cognitive reserve, perhaps reflected
as enhanced levels of neuroanatomical changes, for example,
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Grant et al. Bilingualism, cognitive reserve, and memory
increased gray matter density, white matter integrity, and cortical
thickness (see Li et al., 2014, for a recent review). This assump-
tion would be consistent with the idea of a cognitive reserve-brain
reserve correspondence. On the other hand, there must also be
a behavioral basis for cognitive reserve to arise, perhaps due to
the increased levels of engagement in tasks or activities that rely
on executive control, attention, monitoring, and switching in
bilinguals. This paper aims to provide the missing links between
cognition, brain, and behavior with regard to the cognitive advan-
tages of bilingualism, specifically focusing on how they can be
identified in the aging bilingual brain. We begin by looking at the
behavior and cognition correspondence below, and then discuss
the neural basis of cognitive reserve.
BEHAVIORAL BASIS OF THE BILINGUAL COGNITIVE
ADVANTAGE
EXTENT, NATURE, AND TIMING OF BILINGUAL EXPERIENCE
Unlike many cognitive tasks that may be confined to specific skills
or specific activities, bilingual language experience is typically
intensive, long-term, and practiced on a daily basis with high fre-
quency for most people living in a bilingual environment. It is this
intensity or extent of experience to which researchers attribute
the advantageous cognitive effects of bilingualism. Recent work
from lab training or longitudinal studies has also shown that
the extent of bilingual experience often correlates with lev-
els of L2 proficiency and degree of neuroanatomical changes
(Mechelli et al., 2004;Grogan et al., 2012;Mårtensson et al., 2012;
Schlegel et al., 2012). However, the intensity of experience alone
is not sufficient to account for the unique role of bilingualism.
Two other factors must also be taken into consideration, the
nature of the experience and the timing of it (see Bates, 1999;
Li et al., 2014).
In terms of the nature of bilingual experience, it has been sug-
gested that bilingualism can be compared to a “mental juggler”
(Kroll and Bialystok, 2013). That is, speaking one language often
involves the parallel activation of both of the bilingual’s languages
(i.e., non-selective activation of items from both languages; see De
Groot, 2013 for a recent review), and therefore, inhibitory control
is required to suppress the activation of the non-target language in
the bilingual’s language production or recognition process. This
active use of inhibitory control in bilingualism has been formal-
ized as hypotheses in the Inhibitory Control model (Green, 1998)
and the Bilingual Interactive Activation model (BIA+;Dijkstra
and van Heuven, 2002). To effectively produce or understand
the current speech stream and avoid constant interference from
the unintended language, the bilingual must engage the executive
control system to monitor the two languages and inhibit the acti-
vation of the other language. This is even more important in a
bilingual environment where the speaker has to switch between
languages when conversing with speakers of different language
backgrounds.
In terms of the timing of bilingual experience, while it is true
that in general the earlier a second language (L2) is learned, the
more likely native-like proficiency will be obtained [i.e., the age
of acquisition (AoA) effect; see Hernandez and Li, 2007], it has
now been recognized that very high levels of proficiency in the
L2 is possible even when one learns the L2 late in life. Even
more encouraging is the evidence that the brain shows consid-
erable malleability as a result of language learning experience,
so that both functional and neuroanatomical changes can occur
across the lifespan (see Li et al., 2014 for review). Still, there is
the question of how the timing of language experience interacts
with the intensity or extent and with the nature of the linguis-
tic experience. For example, Abutalebi etal. (2014a) showed that
when older bilinguals in the range of 60–80 years of age are
examined, the AoA effect may not be that important anymore
(i.e., after learning the L2 for 30–50 years, as compared to a
few years of difference in the initial age of L2 exposure). This
situation differs from younger bilinguals (e.g., college students,
our typical experimental subjects) who are in the range of 18–
22 years of age, when a few years of AoA difference can be
significant.
DOMAIN-GENERAL COGNITIVE ENHANCEMENT?
Underlying the bilingual cognitive advantage hypothesis is the
assumption that experience in one domain (bilingualism) can
have a positive impact more broadly across domains (executive
control in general cognition). This is because the bilingual lan-
guage experience engages the executive control system constantly,
in some cases a lifetime experience, in the monitoring, selecting,
controlling, and switching between multiple languages that may be
simultaneously active and competing in the bilingual mind. Such
experiences could in turn sharpen the bilingual mind and lead
to domain-general, non-linguistic enhancement in information
processing (Bialystok and Barac, 2013).
There are several issues that we must resolve before we can
completely embrace this domain-general cognitive enhancement
argument. First, we must link specific aspects of the bilingual expe-
rience with specific components of the executive control system
(see Dong and Li, 2014). This includes the study of the similari-
ties and differences between, for example, language switching and
non-linguistic task switching. A number of studies have now been
devoted to this issue, including the neural substrates of linguistic
versus non-linguistic task differences (e.g., Abutalebi et al., 2008;
van Heuven et al., 2008;Prior and Gollan, 2011). Second, we need
to understand whether language experience is unique in providing
domain-general enhancement in executive control,or whether the
acquisition of other cognitive tasks or skills can similarly lead to
domain-general effects. So far the evidence in this regard has been
scanty, although there has been claim that intensive activities such
as action video games may enhance resource allocation abilities
and hence general cognition (e.g., Bavelier et al., 2012). Related
to this is the challenge of how to separate effects due to bilingual
experience from effects due to other cognitive activities, as well
as from effects of cultural background, language similarity or dis-
tance, education, and socio-economic status, among others (see
Bialystok and Barac, 2013). Third, there is the issue of whether
the cognitive effects of bilingualism are reflected specifically in
the enhancement of executive control abilities, or instead to a
general cognitive processing advantage. Hilchey and Klein (2011)
reviewed a large number of studies and showed that evidence for
bilingual advantages in inhibiting, switching or updating is not
always reliably found. However, bilinguals consistently show faster
RTs overall than do monolinguals (e.g., in both congruent and
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Grant et al. Bilingualism, cognitive reserve, and memory
incongruent trials in the Flanker task), suggesting that it is a gen-
eral processing advantage that characterizes the cognitive benefits
of bilingual experience.
A final issue concerns whether the cognitive advantage of bilin-
gualism depends on the age of the population (see also discussion
of AoA effects in Section “Extent, Nature, and Timing of Bilin-
gual Experience”). For example, robust executive control abilities,
especially inhibitory control as measured by the Flanker task, have
been found with children (e.g., Bialystok et al., 2005;de Abreu
et al., 2012) and older adults (Bialystok et al., 2004,2008), but
often not with young adults (Bialystok et al., 2005;Salvatierra and
Rosselli, 2011;Paap and Greenberg, 2013). Bialystok and Barac
(2013) noted that even when effects of bilingual cognitive advan-
tages are found in young adults, they tend to be more modest in
size than those present in children and older adults, and only under
certain experimental conditions (e.g., more challenging cognitive
tasks; see Costa et al., 2009). In the remainder of this paper, we will
focus on examining the neural mechanisms that underlie bilingual
cognitive advantages in older adults, in an attempt to understand
the relationship between cognitive reserve and brain reserve.
NEURAL BASIS OF BILINGUAL ADVANTAGE IN THE AGING
BRAIN
Given the aforementioned differences in the probability of observ-
ing a bilingual advantage in executive control among differ-
ent age groups, what evidence do we have for the basis of
enhanced executive control abilities in aging bilinguals? How does
this enhancement provide a protective mechanism, i.e., “cog-
nitive reserve,” against age-related cognitive decline in healthy
and abnormal populations? In what follows, we review stud-
ies that point to the positive effects of bilingualism on aging,
and establish the relationship between cognitive reserve and
brain reserve based on extant evidence from the bilingual aging
literature.
COGNITIVE RESERVE, AGE-RELATED DECLINE, AND THE BILINGUAL
EFFECT
In a study surveying hospital records of patients, Bialystok et al.
(2007) identified a sample of 184 patients who were diagnosed
with dementia, most having Alzheimer’s disease. Of these patients,
half were monolinguals (91) and half were lifelong bilinguals (93).
Their analyses showed that these two groups differed significantly:
the bilinguals showed an average delay of 4 years on the age of
dementia onset compared with the monolinguals. To see if such a
difference might have originated from other potentially confound-
ing factors such as education, the authors examined the patients’
occupational status and found that in fact the monolingual group
had more education than the bilingual group, making their results
even more striking, as education has previously been observed to
delay the onset of dementia (Stern, 2009).
These results were subsequently replicated in two other stud-
ies. Craik et al. (2010) collected data from 211 patients who had
suffered from Alzheimer’s disease and found that the lifelong bilin-
guals (102 patients) had experienced symptoms of dementia more
than 5 years later than the monolinguals (109 patients). Again, the
two groups had equivalent cognitive abilities and the monolin-
guals had more education than the bilinguals. Similarly, Alladi
et al. (2013) found an equivalent advantage for bilinguals and
multilinguals over monolinguals in the age of onset of dementia,
including Alzheimer’s, frontotemporal, and vascular dementia2.
Pooling from a large cohort of patients, they found that bilin-
guals (391) showed symptoms of dementia 4.5 years later than
their monolingual (257) counterparts. Moreover, this advantage
was not influenced by potential confounding factors including
education, sex, occupation, or languages spoken.
In addition to delaying cognitive impairment, bilingualism has
also been associated with improving general mental health among
aging populations. For example, Bak et al. (2014) recalled 853
participants (262 bilinguals of varied AoA) who had been first
tested in 1947 as part of the Lothian Birth Cohort and tested them
between 2008 and 2010. Using the data from 1947, they were
able to control for childhood intelligence, gender, socioeconomic
status, and immigration. Overall, they found that bilingualism
provided a protective effect on general intelligence. They also
found that multilingualism, as compared to bilingualism, pro-
vided even more protection with respect to general intelligence,
reading scores, and verbal fluency. Interestingly, the protective
effects on general intelligence and reading were identified regard-
less of age of L2 acquisition, where memory and verbal reasoning
were sensitive to age effects. In conclusion, these studies suggest
that bilingualism contributes to cognitive reserve in both healthy
and disordered aging populations.
STRUCTURAL NEURAL SUBSTRATES OF COGNITIVE RESERVE
In addition to the data from patient records, studies investigat-
ing the effects of bilingualism on cognitive reserve have also used
a variety of neuroimaging methodologies. Given that the differ-
ences observed spanned several measures of structural integrity,
including enhanced gray and white matter as well as enhanced
long-range connectivity in bilinguals compared to monolinguals,
it has been suggested that the enhanced cognitive and neural
functioning in bilinguals may rely upon this enriched neural
architecture.
Luk et al. (2011) assessed functional connectivity changes and
structural brain changes in aging lifelong bilinguals. Bilinguals, as
compared to monolinguals, showed higher white matter integrity
in the corpus callosum projecting to the bilateral superior lon-
gitudinal fasciculi, the right inferior fronto-occipital fasciculus,
and the uncinate fasciculus. In addition, seed-based functional
connectivity centered in bilateral inferior frontal gyri showed sim-
ilar group differences across hemispheres. Specifically, bilinguals
exhibited stronger long-range functional connectivity between the
frontal cortex and posterior regions including occipital and pari-
etal cortex; whereas monolinguals exhibited greater short-range
connectivity mainly centered within the frontal cortex. These
results suggest that lifelong bilingual experience may result in
enhanced processing and integration of information across dis-
parate brain regions, compared to that found in monolinguals.
Highlighting these patterns, the authors suggested that the gray
matter atrophy seen in patients with Alzheimer’s disease may be
compensated for by increased white matter integrity in bilinguals.
2But see Chertkow et al. (2010) for evidence of a multilingual but not bilingual
advantage, and Zahodne et al. (2014) for a discussion of a null result.
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Grant et al. Bilingualism, cognitive reserve, and memory
Increased white matter integrity is an example of brain reserve,
and in this case may form the neural basis for the foundation of
bilingual cognitive reserve.
Abutalebi et al. (2014a) recently observed another form of brain
reserve in bilinguals. They compared gray matter volume (GMV)
of aging monolinguals and late bilinguals. Their analysis found
that although both groups showed effects of aging, bilinguals
showed significantly higher GMV in the left temporal pole (i.e.,
the anterior portion of the left inferior temporal gyrus). In addi-
tion, bilinguals showed higher GMV in the right temporal pole
and bilateral orbitofrontal cortex compared with monolinguals.
However, only the difference in the left temporal pole was sig-
nificantly predicted by performance on an L2 naming task. The
authors argue that the demands exerted by bilingual language
processing affect not only frontal control regions, but also more
posterior (temporal and parietal) areas associated with semantic
processing. Corroborating this argument, Abutalebi etal. (2014b)
showed that Cantonese–English and Cantonese–Mandarin bilin-
guals, compared with monolingual controls, had increased GMV
in the left and right inferior parietal lobule (IPL). The IPL has
been implicated in lexical representation, semantic integration,
and phonological working memory, and increased GMV in this
region could be attributed to the bilingual’s experience with a
large new vocabulary in the L2 (Mechelli et al., 2004;Richard-
son and Price, 2009;Della Rosa etal., 2013;seeLi et al., 2014 for
reviews).
In contrast with the results observed by Luk et al. (2011),Gold
et al. (2013a), and Abutalebi et al. (2014a,b) found that bilin-
guals exhibited cognitive, rather than brain, reserve. That is, in
their DTI and VBM analyses of 20 healthy lifelong bilinguals
and 63 healthy monolinguals, they found that the two groups
showed no difference in GMV, and that the bilinguals actually
showed decreased levels of white matter integrity (as measured
by fractional anisotropy and radial diffusivity) than the mono-
linguals. Despite these structural deficits, the bilinguals were able
to perform equivalently to the monolinguals on a range of tasks,
including IQ, working and episodic memory, and task switching.
This pattern of results precisely fits the definition of cognitive
reserve: equal performance in the face of structural pathology
(Stern, 2009). The authors interpret these results as being poten-
tially due to a higher incidence of pre-clinical Alzheimer’s disease
within their sample, especially given that they observed deficits
in white matter tracts (specifically within the inferior longitu-
dinal fasciculus/inferior fronto-occipital fasciculus) commonly
affected by Alzheimer’s disease. Interestingly, the authors note
that the tracts associated with the executive control network
ranging from the lateral frontal cortex back to the parietal cor-
tex (e.g., the superior longitudinal fasciculus and anterior limb
of the internal capsule) were largely preserved in their bilingual
group.
Further support for this link between bilingualism and cogni-
tive reserve comes from the only study that examined functional
differences between aging bilinguals and monolinguals (Gold et al.,
2013b). They found that older bilinguals (the same sample from
Gold et al., 2013a) showed less activity in several frontal regions
in association with smaller proportional switch costs compared to
age-matched monolinguals, although both groups showed more
frontal activation than the younger comparison groups. The com-
bination of reduced neural recruitment and improved cognitive
performance is often characterized in the aging field as reflecting
greater neural efficiency in high vs. low performing individuals
(Rypma et al., 2005,2006;Grady, 2008).
To review, the structural and functional imaging results, consis-
tent with previous patient data reviewed so far, suggest that brain
differences between bilinguals and monolinguals may underlie
group differences associated with enhanced cognitive function-
ing in older bilingual, as compared with monolingual, adults.
These structural and functional effects extend across the lan-
guage and executive control networks, which overlap in keys
areas including the prefrontal cortex (PFC), IPL, anterior cin-
gulate cortex, and basal ganglia (Hervais-Adelman et al., 2011).
Importantly, the neural networks associated with bilingualism
overlap considerably with the neural networks that commonly
decline in aging (see discussion below on the overlap between
memory and language systems). Such extensive consequences
of bilingual experience on the brain’s anatomical architecture
and cognitive processing are both unique and important in that
they reflect the results of a lifelong experiential context juggling
multiple languages, a process that involves both language con-
trol and executive control. Compared with most other training
experiences that typically produce positive results in a single
domain, the bilingual experience seems to have far-reaching
consequences for the mind and the brain (Dye et al., 2009;
Kroll and Bialystok, 2013).
BILINGUAL COGNITIVE ADVANTAGES: PERSPECTIVES FROM
MEMORY AND AGING
Given the extent to which the bilingual experience appears to
affect the brain as discussed in Section “Neural Basis of Bilin-
gual Advantage in the Aging Brain,” it is surprising that bilingual
memory performance remains relatively understudied to date.
It is even more surprising when one considers the amount of
media attention that research on the protective effects of bilin-
gualism has received, especially the studies onAlzheimer’s disease,
a disease that primarily affects memory (Dubois et al., 2007). In
addition, studies of memory, especially episodic memory and
retrieval, have shown that recollection commonly elicits activ-
ity not only in the medial temporal lobe (MTL), but also the
frontal executive systems and the sensory areas associated with
the memory being retrieved, suggesting considerable overlap
between the areas associated with memory and those associ-
ated with bilingual brain reserve (Dobbins and Davachi, 2006).
This link is further supported by the existence of overlapping
brain regions involved in both memory and language more gener-
ally. For example, Rodríguez-Fornells et al. (2009) hypothesized
that the MTL is critical for initial word learning in the sec-
ond language, and data from other studies are consistent with
this hypothesis. Mårtensson et al. (2012) found that hippocam-
pal volume increased after intensive training in simultaneous
interpreting, as did cortical thickness of the left PFC (specif-
ically the inferior frontal gyrus), a region that has also been
implicated in encoding success (Rizio and Dennis, 2013). In addi-
tion, Stein et al. (2012) and Hosoda et al. (2013) both found
increases of gray matter density in the left anterior temporal
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Grant et al. Bilingualism, cognitive reserve, and memory
lobe (ATL), an area critical for verbal memory (Bonelli et al.,
2013), and the increases positively correlated with the learner’s
proficiency level in the L2. The close language-memory relation-
ship has led some researchers to propose that foreign language
learning should be explored as a potential treatment to build
cognitive reserve in the elderly (e.g., Antoniou et al., 2013). It
is also critical, however, to examine the relationship between
bilingualism and memory systems in the current bilingual elderly
population, as memory research in older adults has the poten-
tial to help us understand not only the bilingual advantage as
it applies to healthy aging, but also to aging-related cognitive
declines.
THE POSTERIOR-TO-ANTERIOR SHIFT IN AGING (PASA) HYPOTHESIS
One specific hypothesis that aids us in making the link between
memory and bilingualism is posterior-to-anterior shift in aging
(PASA), a hypothesis based on functional neuroimaging studies of
memory and aging (see Figure 1 below;forareviewseeDennis
and Cabeza, 2008).
The PASA pattern of results has been observed across many
cognitive tasks in healthy aging (see review in Dennis and Cabeza,
2008). To understand the consequences of the PASA, we need
to understand that recollection is commonly associated with
activity in frontal executive systems and the sensory areas asso-
ciated with that experience (e.g., fusiform gyrus activity for the
memory of a face), as well as the MTL (Dobbins and Davachi,
2006). PASA’s basic hypothesis is that in normal healthy aging,
at least for the monolingual speakers, older adults, compared to
younger adults, exhibit age-related decreases in neural activity
in posterior sensory areas of the cortex, while at the same time
show increases in PFC [especially dorsolateral prefrontal cortex
(DLPFC)] activity. PASA is generally considered a form of neu-
ral compensation in aging, given that this increased reliance on
frontal instead of posterior cortical regions allows the older adults
to preserve cognitive performance at a level comparable to younger
adults.
Within the aging population, enhanced functioning in bilin-
guals (compared to monolinguals) is consistent with the PASA
hypothesis. Previous research (e.g., Ossher et al., 2013) has focused
on the role of bilingualism in enhancing the frontal systems
involved in executive function, thus allowing for greater cogni-
tive reserve in bilingualism and memory. Although the frontal
activity observed in PASA is characterized as compensatory for
reduced activation in the posterior brain regions, the bilingual
aging studies reviewed so far suggest that bilingual experience
serves as another compensatory mechanism to help mitigate age-
related declines by not only engaging the frontal systems, but also
preserving structures in posterior areas of the cortex and their
connections with the frontal cortex. That is, although monolin-
gual older adults experience the posterior to anterior shifting, in
bilingual aging adults, the posterior regions have not declined
as substantially, and hence bilinguals show less of the actual
shifting in the PASA patterns as in monolinguals. Recent results
from Abutalebi et al. (2014a,b) support this preservation hypoth-
esis, with an emphasis on the temporal and parietal regions. As
mentioned earlier, Abutalebi et al. (2014a,b) found that aging
bilinguals showed enhanced GMV compared to aging monolin-
guals in the left ATL and in the IPL. Moreover, unlike monolinguals
who rely mainly on the frontal cortex to compensate for per-
formance compromised by aging, bilinguals also preserve the
frontal-posterior connectivity in addition to the functioning of
the posterior regions. For example, Luk et al. (2011) found that
aging monolinguals exhibited connectivity patterns congruent
with PASA at rest, but aging bilinguals showed greater connec-
tivity between the IFG and posterior areas including the middle
temporal and occipital gyri, precuneus, the right IPL, and the
caudate.
ROLE OF THE PFC AND FRONTAL-POSTERIOR AND FRONTAL-BASAL
GANGLIA CONNECTIVITY
The extant evidence so far suggests that aging bilinguals exhibit
preserved GMV in the posterior regions (in particular the tem-
poral and parietal regions) and enhanced connectivity between
the PFC and posterior regions (Luk et al., 2011;Abutalebi et al.,
2014a,b). Given this evidence, we propose that the enhancement of
PFC function, along with preserved temporal cortex and increased
FIGURE 1 |Posterior-to-anterior shift in aging (PASA) predicts that with age comes a shift, such that older participants show greater activity in the left
dorsolateral prefrontal cortex (DLPFC) and less activity in the left visual cortex during memory tasks, while younger adults show the reverse pattern.
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Grant et al. Bilingualism, cognitive reserve, and memory
FIGURE 2 |An illustration of the monolingual vs. bilingual aging brain.
In monolinguals, aging is associated with an increased reliance on the
frontal regions, according to the PASA hypothesis. In bilinguals, the aging
brain shows preservation of the posterior regions (including temporal and
parietal cortex), as well as increased connectivity between frontal and
posterior areas, leading to cognitive reserve.
frontal-posterior connectivity may underlie the brain reserve of
bilingualism. Figure 2 illustrates this proposal.
Our proposal is consistent with a recent model by Stocco
et al. (2014) that describes how the executive control advan-
tage may develop in the framework of the conditional routing
model. According to Stocco etal. (2014), the basal ganglia act
to increase the strength of the cortical connections that would
otherwise have not been selected due to lower resting activation
(see Figure 3). Stocco et al. (2014) argued that language switch-
ing is a process analogous to picking the connection with lower
resting activation. Because bilingualism by necessity involves lan-
guage switching, the authors suggested that bilingualism improves
top–down control ability, which includes both language control
and general cognitive control. This model is congruent with
a number of neuroimaging studies implicating the basal gan-
glia and specifically the caudate nucleus as being critical for
language and cognitive control (e.g., Crinion et al., 2006;Tan et al.,
2011), as well as a recent neuropsychological study that found
direct evidence via intra-operative electrical stimulation of the
role of the left caudate in both language and cognitive control
(Wang et al., 2013). To summarize, the conditional routing model
suggests that the role of the basal ganglia is to strengthen previ-
ously established connections in order to over-ride the currently
most active connection, as is necessary during language or task
switching.
As we suggested earlier, these benefits should also sup-
port memory performance. Specifically, enhancement of frontal
regions should allow for the preservation of memory skills
involving executive control, such as recollection, while brain
reserve in posterior cortical regions and improved long-range
connectivity may enhance older bilinguals’ ability to encode
and retrieve details of past events, a function that is typi-
cally impaired in healthy aging (e.g., Park et al., 2004;Dennis
et al., 2007;Gutchess et al., 2007). While monolinguals compen-
sate for reduced long-range connectivity with increased short-
range connectivity and activity within the frontal cortex (i.e.,
PASA; Dennis and Cabeza, 2008), the research that we have
reviewed so far suggests that aging bilinguals compensate less
drastically in this manner than aging monolinguals (Luk et al.,
2011;Gold et al., 2013a). We suggest that this reduced PASA
shift in bilinguals is due to their enhancements in the poste-
rior regions (e.g., the medial temporal regions, the temporal
pole, and inferior parietal cortex), as well as the connectivity
between these areas with the PFC and with the basal ganglia
(Stocco et al., 2014).
THE ROLE OF EXECUTIVE CONTROL AND BRAIN RESERVE IN EPISODIC
MEMORY RETRIEVAL
Examined against the above proposal, brain reserve resulting
from bilingualism not only supports executive control tasks, but
FIGURE 3 |The conditional routing model, adapted from Stocco
et al. (2014).In this figure, Side 1 represents a prototypical situation,
where prefrontal cortex (PFC) is receiving multiple concurrent signals.
In this situation, the strongest concurrent signal (from region B) is
most likely to affect the PFC (hence the figure shows the impact of
connection B in the prefrontal cortex). Side 2 exemplifies the role of
the basal ganglia, which serves as a mechanism to modify cortical
pathways. In this case, the basal ganglia strengthen the signal
particularly from area C (hence the figure features the impact of
connection C).
Frontiers in Psychology |Language Sciences December 2014 |Volume 5 |Article 1401 |6
Grant et al. Bilingualism, cognitive reserve, and memory
memory functioning as well. Although there are as yet no neu-
roimaging studies investigating this relationship, a small, but
growing, literature has examined memory performance in older
bilinguals at the behavioral level. Results from these studies have
the potential to help us understand the nature of bilingual brain
reserve and its relationship to the incidence and progression of
dementia.
One of the first studies in this area by Wodniecka et al. (2010)
found that older bilinguals are advantaged at particularly diffi-
cult recollection memory tasks compared to older monolinguals,
although younger participants (monolingual and bilingual) out-
performed both older groups. At the same time, there was no
difference between older monolinguals and bilinguals’ ability to
remember familiar items. This distinction is important because
recollection memory, in particular, requires the use of executive
control to select the specific details of the memory over the gist
content, whereas familiarity is characterized by an inability to
remember details despite a feeling that the item has been seen
before. These results consequently suggest that the bilingual exec-
utive control advantage does indeed extend to memory, as they
found that bilinguals were selectively advantaged in recollection
as opposed to familiarity judgments.
Further evidence for the role of bilingualism on memory per-
formance comes from another study by Ljungberg et al. (2013).
Similar to Bak et al.’s (2014) longitudinal study that found pre-
served memory performance among early bilinguals (see Cog-
nitive Reserve, Age-Related Decline, and the Bilingual Effect),
Ljungberg et al. (2013) presented a compelling case for a bilingual
advantage in episodic memory in the form of a 20-year longitu-
dinal study. Participants were primarily late bilinguals matched
on nationality, gender, education, and general intelligence, rang-
ing from ages 35 to 70 at the first testing session. Their data
was drawn from a larger study, the Betula Prospective Cohort
Study, and included performance on three types of recall tasks, as
well as letter and category fluency. Ljungberg et al. (2013) found
that bilinguals were significantly advantaged on the episodic recall
tasks, and that this advantage did not interact with age. A sim-
ilar advantage was found for letter, but not category, fluency.
While category fluency allows for one to select items relatively
freely from one’s existing semantic network, letter fluency requires
that one inhibit semantic and occasionally phonological connec-
tions in order to recall other words that fit the orthographic
criterion, and consequently can be interpreted as an executive
control task (see Martin et al., 1994). In short, Ljungberg et al.
(2013) found an advantage for bilinguals in episodic recall that co-
occurred with increased performance on another executive control
task.
Inarecentstudy,Schroeder and Marian (2012) further repli-
cated the pattern of results from the above two studies that
shows benefits of bilingualism for recollection memory under
conditions requiring executive control. They found that older
bilinguals (AoA of approximately 15) performed better than
older monolinguals on an episodic memory retrieval task. This
task required them to remember specific aspects of scenes,
which requires executive control via the inhibition of the gist
of the scene. Critically, there was also a correlation between the
results on that task and the Simon task, a common measure
of executive control. Specifically, the bilinguals’ accuracy on
the Simon task was positively correlated with the number of
scenes recalled. The monolinguals showed a similar correlation,
but the correlation was non-significant. Schroeder and Mar-
ian (2012) interpreted these results to suggest that bilinguals’
better performance on the episodic memory task was due to
improved executive control abilities. The authors went on to sug-
gest that bilinguals’ “extra reliance on the MTL memory system
may exercise and enhance its functioning” (p. 9), allowing for
better recall. Although Schroeder and Marian (2012) did not
have neuro-imaging data to support this idea, there is support
for the hypothesis that the neural basis of the bilingual advan-
tage might involve the temporal and parietal cortex, as has been
discussed.
CONCLUSION AND FUTURE DIRECTIONS
The studies of bilingual memory to date appear to suggest that
bilinguals do show an advantage for aspects of memory that
require executive control, such as episodic and verbal recall. As
discussed in Section “Bilingual Cognitive Advantages: Perspec-
tives from Memory and Aging,” we propose that this advantage
may stem from two complimentary mechanisms, a frontal advan-
tage and an advantage in making long-range connections between
the PFC and posterior areas of the cortex, which are critical for suc-
cessful recollection (Dobbins and Davachi,2006). As illustrated in
Figure 2, these two mechanisms work differently in monolinguals
versus bilinguals, due to their differential experience with language
control. As language selection and retrieval occur not only in the
frontal cortex, but also in the temporal and parietal cortex (e.g.,
Abutalebi et al., 2008,2014a,b), we expect to see strengthening of
both frontal and temporal cortical pathways as a result of bilin-
gualism. Current theories of semantic memory have implicated
the temporal and inferior parietal cortex as convergence zones
for the storage of representations (for a review, see Binder and
Desai, 2011), and the understanding of the connectivity between
these regions and the executive control system present an exciting
opportunity for new research in bilingualism.
Thus, the studies of aging and memory in monolinguals com-
pared with bilinguals provide a bridge for understanding the
bilingual advantage in executive control and the cognitive reserve
against Alzheimer’s dementia that has been observed in bilingual
populations (e.g., Craik et al., 2010;Alladi et al., 2013). On the
one hand, the enhanced executive control ability provides the
basis for increased cognitive reserve, and on the other, cogni-
tive reserve is sub-served by brain reserve in terms of increased
neuroanatomical integrity or density. The analyses presented in
this paper only represent an initial attempt at identifying the rela-
tionships among bilingual language experience, executive control,
episodic memory, and the mechanisms that support the bilingual
advantage through cognitive reserve and brain reserve.
Our analyses so far suggest that bilinguals’ cognitive and brain
reserves share the same mechanism as their advantaged execu-
tive control processing, for example, in the bilinguals’ use of the
basal ganglia to strengthen weaker cortical circuits (Stocco et al.,
2014). Such strengthening leads to functional and structural con-
sequences, such as increased white matter and gray matter. These
structural changes are suggestive of synaptogenesis and dendritic
www.frontiersin.org December 2014 |Volume 5 |Article 1401 |7
Grant et al. Bilingualism, cognitive reserve, and memory
morphology (in the case of gray matter) and increased myelina-
tion (in the case of white matter), which allows for more efficient
signal communication (see Antoniou et al., 2013;García-Pentón
et al., 2014;Li et al., 2014). The large scale of the networks associ-
ated with bilingualism makes such improvements critical to allow
for fluent speech, and the overlapping nature of this network
(between bilingualism and the executive control network) makes
it likely that such benefits due to bilingualism would translate into
both executive control benefits and consequently,brain reserve for
aging-related memory decline.
Future research is needed to elucidate the mechanisms of bilin-
gualism and its cognitive and neural substrates. To understand
the implications of functional connectivity between frontal cor-
tex and posterior cortical areas on memory, we need to conduct
studies examining functional connectivity in younger and older
bilinguals while they complete memory tasks. Such experiments
would potentially allow for the differentiation and specification of
the role of each of the types of reserve due to bilingualism, that
is, structural connectivity and volume in the executive function
network. Our general prediction is that like healthy monolinguals,
aging bilinguals will exhibit a PASA pattern of neural recruitment
compared to young adults during memory and other cognitive
tasks. Future experiments comparing young and aging bilinguals,
as opposed to only aging monolinguals and bilinguals, will be
critical to establish such a parallel.
Another important direction would to be conduct longitudinal
research to track the use and development of multiple languages.
As we mentioned in Section “Extent, Nature, and Timing of Bilin-
gual Experience,” acquiring a second language appears to have
profound structural impacts on the brain (e.g., Mårtensson et al.,
2012;Della Rosa et al., 2013;seeLi et al., 2014 for review). However,
the only longitudinal study of memory performance in bilinguals
to date (Ljungberg et al., 2013) has focused on behavioral perfor-
mance, as reviewed above. Consequently, we do not yet know how
the bilingual brain changes over time on tasks that tap into long-
term or working memory. Understanding such changes in healthy
aging bilinguals and monolinguals and the differences between
them will help us to better understand not only cognitive reserve,
but also abnormal aging in general.
A final promising line of research could be the study of the
effects of foreign language training on memory in older adults.
Antoniou et al. (2013) recently called for such a training program
in order to explicate the role of bilingualism in cognitive reserve,
especially relating to executive control tasks. As we have suggested
in this paper, however, executive control appears to have a signifi-
cant influence on memory as well, and given the results suggesting
that older adults also show gray matter changes in response to
training (Lövdén et al., 2013) we agree that such a study could be
extremely informative not only regarding the cognitive reserve of
executive control abilities, but also of memory. If, as we predict,
such a study would show either enhanced or preserved mem-
ory abilities, as well as executive control abilities, the implication
would be that the findings of bilingual cognitive reserve in the face
of dementia are in fact related to enhancements of the cognitive
control system.
In conclusion, research in the junction of bilingualism, mem-
ory, and cognitive and brain reserve can provide significant
insights into current debates on bilingual cognitive advantages.
Based on the current neuroimaging evidence concerning the bilin-
gual advantage in older adults and on models of aging and
memory, we suggest examining brain reserve in not just the frontal
cortex, but also its connectivity with the temporal, parietal, and
subcortical areas, and how these neural correlates underlie the
cognitive reserve in older bilinguals to protect against age-related
cognitive declines.
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Conflict of Interest Statement: The authors declare that the research was conducted
in the absence of any commercial or financial relationships that could be construed
as a potential conflict of interest.
Received: 17 June 2014; paper pending published: 07 October 2014; accepted: 16
November 2014; published online: 03 December 2014.
Citation: Grant A, Dennis NA and Li P (2014) Cognitive control, cognitive
reserve, and memory in the aging bilingual brain. Front. Psychol. 5:1401. doi:
10.3389/fpsyg.2014.01401
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Psychology.
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