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The role of cognitive reserve in cognitive aging:

Results from the neurocognitive study on aging
a

Erasmia Giogkaraki , Michalis P. Michaelides & Fofi Constantinidou

a

Department of Psychology, University of Cyprus, Nicosia, Cyprus

Center for Applied Neuroscience and Department of Psychology, University of

Cyprus, Nicosia, Cyprus
Published online: 18 Oct 2013.

To cite this article: Erasmia Giogkaraki, Michalis P. Michaelides & Fofi Constantinidou (2013) The role of cognitive
reserve in cognitive aging: Results from the neurocognitive study on aging, Journal of Clinical and Experimental
Neuropsychology, 35:10, 1024-1035, DOI: 10.1080/13803395.2013.847906
To link to this article: http://dx.doi.org/10.1080/13803395.2013.847906

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Journal of Clinical and Experimental Neuropsychology, 2013

Vol. 35, No. 10, 10241035, http://dx.doi.org/10.1080/13803395.2013.847906

The role of cognitive reserve in cognitive aging: Results

from the neurocognitive study on aging
Erasmia Giogkaraki1 , Michalis P. Michaelides1 , and Fofi Constantinidou2
1

Department of Psychology, University of Cyprus, Nicosia, Cyprus

Center for Applied Neuroscience and Department of Psychology, University of Cyprus, Nicosia,
Cyprus

Downloaded by [187.141.45.19] at 12:11 21 August 2014

(Received 10 April 2013; accepted 19 September 2013)

The study tested the cognitive reserve hypothesis by quantifying cognitive reserve (CR) and subsequently determining its role in executive function and verbal episodic memory performance. A neuropsychological battery was
administered to 383 Greek-Cypriot older adults. A multiple indicators multiple causes (MIMIC) latent construct
was utilized to define CR incorporating three indicators: years of education, vocabulary, and reading performance.
Findings from two structural equation models supported the moderating role of CR in reducing the direct negative
effect of age on verbal episodic memory and on executive function. The study illustrates a parsimonious way of
defining CR and provides empirical support for the CR hypothesis.
Keywords: Aging; Cognitive reserve; Education; Episodic memory; Executive function.

Aging is associated with cognitive decline and

increased risk of dementia. Cognitive decline is a
central feature for understanding the aging process. Individual trajectories of cognitive change are
highly heterogeneous, with some declining rapidly
and others declining slowly or even improving
(Reed et al., 2010; Wilson et al., 2002). Additionally,
dissociation between brain pathology and clinical expression is observed (Satz, Cole, Hardy, &
Rassovsky, 2011). The concept of reserve provides
a framework for explaining the above individual
differences (Stern, 2011).
Reserve has two forms: brain reserve and cognitive reserve (CR). Brain reserve and CR are
considered as independent, as well as interactive in

explaining individual differences in cognitive and

functional resilience of brain pathology (Tucker &
Stern, 2011). Brain reserve is defined as the brains
capacity to sustain a certain amount of pathological change before the emergence of the associated
clinical symptoms (Brickman et al., 2011; Satz,
1993; Stern, 2002). According to the brain reserve
hypothesis, the quality of development in early life
(Little, Busschang, Pena Reyes, Tan, & Malina,
2006; Wadsworth, Hardy, Paul, Marshall, & Cole,
2002) may provide resistance against the development of brain pathology (Brickman et al., 2011).
CR can be defined as the ability to use alternate cognitive strategies, in order to optimize or maximize
performance on cognitive tasks (Baldivia, Andrade,

The authors would like to thank the many volunteers and their families for participating in this project. We are indebted to the staff
from the many adult community centers who assisted our research team in the recruitment of study participants and facilitated our
extensive testing processes, especially Kallia Sophocleous and Anna Filippou from the Strovolos Municipality, Sophia Metti from the
Lacadamia Municipality, Panagiotis and Christina Karamani from Nicosia Municipality, Elena Theodoulidou Polidorou from Ayios
Dometios Municipality, and the staff from EOKA Veterans Association and the Cypriot Retiree Union (EKYSY). Additionally, we are
very thankful to the many researchers in the Neurocognitive Research Laboratory at the University of Cyprus who participated in the
data collection and data management, and especially Juliana Prokopiou who manages the Neurocognitive Study on Aging.
This work was funded by the Cyprus Research Promotion Foundation through grant awarded to Fofi Constantinidou
ANPITIKE/KOIN/0308(BE)/07 and NEA YOOMH/TPATH/0309/37.
Address correspondence to: Erasmia Giogkaraki, Department of Psychology, University of Cyprus, 65 Kallipoleos St., P.O.
Box 20537, 1678, Nicosia, Cyprus (E-mail: erasmia.yogaraki@gmail.com).

2013 Taylor & Francis

Downloaded by [187.141.45.19] at 12:11 21 August 2014

COGNITIVE RESERVE IN AGING

& Bueno, 2008). The CR hypothesis explains why

those with higher IQ, education, occupational
attainment, or participation in leisure activities
evidence less severe clinical or cognitive changes
in the presence of age-related or even Alzheimer
Disease (AD) pathology (Tucker & Stern, 2011,
p. 354). According to the CR hypothesis, individuals with higher reserve are able to cope with brain
pathology through some form of active compensatory strategy better than those with lower reserve.
Therefore CR is hypothesized to moderate the association between brain pathology and the expression of the pathology rather than protecting the
brain against the development of brain pathology
(Brickman et al., 2011; Singh-Manoux et al., 2011).
In other words, greater CR allows individuals to
cope better with the cognitive changes associated
with aging, by promoting more flexible usage of
cognitive processes, such as new strategies. The
present study is part of the first longitudinal project
on cognitive aging in Cyprus, the Neurocognitive
Study on Aging (Constantinidou, Christodoulou,
& Prokopiou, 2012). Although brain reserve is an
important theoretical construct in its own right,
the purpose of the current study was to propose a
definition of the CR construct, in order to examine the cognitive reserve hypothesis on a large
cohort of healthy aging adults in association with
age and cognitive functions. We refer to CR as a
distinct construct that represents a meaningful distinct dimension of individual differences in aging
(Siedlecki et al., 2009).
Cognitive reserve is often conceptualized as a
capacity that is progressively built through cognitively demanding and stimulating experiences, such
as education (Reed et al., 2010). In fact, years
of formal education seems to be the most widely
studied variable, and it is commonly used as the
single proxy for the concept of CR (Valenzuela &
Sachdev, 2006a, 2006b). The theoretical rationale
for using formal education as a proxy measure of
cognitive reserve is based on the assumption that
it generates new cognitive strategies (Stern, 2002).
Other single proxy measures could be occupational
status or other socioeconomic status variables, premorbid IQ, and mental activities (Valenzuela &
Sachdev, 2006b). An important limitation of the
single proxy approach is that most single measures
of CR may be linked to neuropsychological test performance through many alternative paths and not
only through the hypothesized reserve mechanisms
(Jones et al., 2011).
Alternatively, CR could be conceived as a hypothetical factor, not directly measured by a single
measure, but as a latent construct (Jones et al.,
2011; Stern, 2006; Whalley, Deary, Appleton, &

1025

Starr, 2004). Latent variable data analysis approach

might help to test theories regarding the role of CR,
at least until a direct measure is identified. Jones
and colleagues (2011) support a multiple indicator
model, inferring that the latent variable reserve
may have several advantages. First, it may be a more
precise measure of reserve than those obtained with
any single indicator. Moreover, it may avoid some of
the limitations of the nonreserve pathways of interaction with cognitive measures. Finally, it could
help summarize the relationship between reserve
and a cognitive function with a single coefficient.
In the present study, we propose a latent construct of CR, drawing on information from educational attainment and estimates of crystallized
ability. Each of these variables has been used in
the literature as a single proxy of CR because
they reflect life experiences that could potentially
protect against clinical manifestation of brain disease (Siedlecki et al., 2009). Receptive vocabulary
appears to be a good indication of crystallized
knowledge and is typically tested in passive vocabulary tasks. Constantinidou, Christodoulou, et al.
(2012) demonstrated that while education can affect
receptive vocabulary performance, this ability is
resistant to age as measured in two groups of
matched older adults ages 6575 and 76+ years.
The present study included receptive vocabulary
performance in the development of the proposed
CR latent construct. In contrast, the study incorporated cognitive measures that are sensitive to the
changes of biological aging processes as outcomes.
Research indicates that changes in cognitive performance associated with aging are probably a
result of the dynamic neurobiological processes
that occur during the brain development across
the lifespan. These processes seem to be selective,
affecting different areas of the brain at different rates. Prefrontal cortical areas, inferior temporal lobe areas, and the hippocampus sustain the
greatest diminution of blood flow, neuronal loss,
and shrinkage (Kramer, Mungas, & Reed, 2007).
Furthermore, the availability or reuptake efficiency
of certain neurotransmitters seems to be affected
by age, which in turn can result in a decrease in
the speed of synaptic signal transmission (Wu, Oh,
& Distenhoft, 2002). The above neuropathological
changes provide a framework for understanding
the cognitive changes observed with aging because
the aforementioned areas and associated networks
are critical for organizing, categorizing, learning, and retrieving information (Constantinidou &
Baker, 2002; Constantinidou, Christodoulou, et al.,
2012; Glisky, Polster, & Routhieaux, 1995; Lee,
Yuen, Chu, & Chi, 2004; Salthouse & Ferrer-Caja,
2003).

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GIOGKARAKI, MICHAELIDES, CONSTANTINIDOU

The present work focuses on two neuropsychological domainsepisodic memory and

executive functionthat are associated with the
above neurobiological changes in aging. Episodic
memory can be affected by normal aging and
by multiple brain disorders; hence, it is a sensitive marker of pathological aging (Brickman &
Stern, 2009; Christensen, 2001; Reed et al., 2010).
Executive function as a neuropsychological construct is commonly associated with the frontal-lobe
hypothesis of aging. The frontal-lobe hypothesis
predicts that age-related changes should be more
observable in tasks involving executive control than
in tasks with lesser control demands. Cortical control is supported largely by circuits in the prefrontal
lobes and particularly dorsolateral prefrontal lobe
networks, which are vulnerable to the aging process
(Constantinidou, Wertheimer, Tsanadis, Evans, &
Paul, 2012; Span, Ridderinkhof, & van der Molen,
2004).
Additionally, studies reveal executive function
and episodic memory as distinct factors accounting for age-related changes in cognition (Glisky
et al., 1995; Salthouse & Ferrer-Caja, 2003). These
differential effects may arise from separate aging
processes on frontal-striatal circuits and on the
medial temporal lobe memory system (Buckner,
2004). Moreover, distinct white matter hyperintensity loci are associated with lower executive function scores and episodic memory scores (Smith
et al., 2011). However, these two cognitive domains
are not completely independent, as there is evidence that they are correlated. Executive function is
thought to interfere with the successful engagement
in the acquisition and the retrieval of information (Stuss & Alexander, 2000). Studies in normal
aging showed that deficits in executive function
have an indirect impact on memory performance
(Crawford, Bryan, Luszcz, Obonsawin, & Stewart,
2000; Salthouse & Ferrer-Caja, 2003). Given the
effects of aging on executive function and episodic
memory performance, both of these abilities were
incorporated as outcome variables in our proposed
model.
The purpose of this study was to propose
a definition of the CR construct, in order to
examine the CR hypothesis on a large cohort
of healthy aging adults in association with age
and cognitive functioning. We tested the CR
hypothesis on two main cognitive domains: verbal episodic memory and executive function.
A latent variable model was implemented to test
the hypothesis stating that CR plays a moderating role in the relationship between age and both
episodic memory and executive function in healthy
aging.

METHOD
Participants
Participants for this study were recruited from
the Neurocognitive Study for the Aging, a longitudinal project exploring neuropsychological
neurocognitive performance, health indices, and
biological markers, as well as quality of life issues
in elderly Greek Cypriot community volunteers.
The study was conducted in compliance with
the Helsinki Declaration and was approved by
the National Bioethics Committee, Republic of
Cyprus. Volunteers were recruited from major districts in Cyprus that include Nicosia, Limassol,
and Paphos. Out of the 483 participants in the
database, 383 Greek-Cypriot adults (182 males
and 201 females, ranging in age from 60 to
92 years) met the inclusion/exclusion criteria for
this study. The demographic distribution (age, gender, and education) of the study is in line with the
Cyprus Government census data (Cyprus Statistical
Service, 2009). Table 1 presents the group demographics.
The inclusion criteria for all participants were the
following: (a) native Greek speakers, (b) males and
females of age 60 and above, (c) good general health
with no previous history of neurological disorder
such as head trauma, stroke, or neurodegenerative disorder, (d) no history of severe psychiatric
or emotional disorder requiring hospitalization, (e)
Mini-Mental State Examination (MMSE) score of
23 or higher, and (f) Geriatric Depression Score
(GDS) of 9 or lower. Moreover, we included in the
analysis the participants that we were assured were
functional in their daily activities.

Procedure
Participants were administered a battery of
neurocognitive and language tests (translated
and adapted into Greek and previously used in
other research studies) to assess certain aspects
of cognitive and language functioning. Research
data established that these tests are sensitive to
cognitive decline (Constantinidou, Christodoulou,
et al., 2012; Greenlief, Margolis, & Erker, 1985;
Lezak, Howieson, & Loring, 2004; Margolin, Pate,
Friedrich, & Elia, 1990; Pfeffer et al., 1981). Below
are the measures included in the study:
General cognitive screening
Mini Mental Status Examination (MMSE;
Fountoulakis, Tsolaki, Chantzi, & Kazis, 2000).

COGNITIVE RESERVE IN AGING

TABLE 1
Participants demographic characteristics and scores on
neuropsychological measures
Measure

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Age (years)
Education (years)
Vocabulary
Reading pseudo
HVLT1
HVLTimmediate
HVLTdelayed
LMimmediate
LMdelayed
TMTA (s)
TMTB (s)
SDMT
Fluency category
Phonemic fluency

Mean

SD

Range

73.328
7.898
18.678
59.590
4.324
17.214
4.317
10.000
6.611
88.643
213.932
21.455
10.448
8.133

6.363
4.176
7.173
12.062
1.673
5.085
2.880
3.925
3.891
40.226
105.174
10.060
3.066
3.432

6092
021
031
0110
09
430
012
019
019
30369
53755
051
228
125

Note. Vocabulary: number of correct responses in the Greek version of the Peabody Picture Vocabulary Test (PPVTIII; Simos
et al., 2011); Reading pseudo: the number of total pseudowords
read correctly in 45 s (Simos et al., 2013); HVLT: Greek version of the Hopkins Verbal Learning TestRevised (Benedict
et al., 1998; adapted in Greek by Constantinidou upon permission from the publisher); HVLT1: the number of recalled words
in the first trial; HVLTimmediate: the total number of words
immediately recalled in the three learning trials; HVLTdelayed:
the number of words recalled in the delayed recall trial; LM:
Story A of Logical Memory subtest from Wechsler Memory
ScaleRevised (Wechsler, 1997); LMimmediate: the score in the
immediate recall; LMdelayed: the score in the delayed recall;
TMT: Trail Making Test; TMTA: time in seconds for the TMT
Part A; TMTB: time in seconds for the TMT Part B; SDMT:
the correct responses in 90 s in the Symbol Digit Modalities
Test (Smith, 1982); Fluency category: the number of the correct words generated in 60 s for the category animals; Phonemic
fluency: the number of correct words starting with the letter F
generated in 60 s.

Depression screening
Geriatric Depression Scale (GDS; Fountoulakis
et al., 1999).
Executive function tests
Trail Making Tests (TMT) A and B (Constantinidou, Papacostas, Nicou, & Themistocleous,
2008; Zalonis et al., 2008): The TMT provides information on visual search, scanning, speed of processing, mental flexibility, and executive functions.
Originally, it was part of the Army Individual Test
Battery (1994) and subsequently was incorporated
into the HalsteadReitan Battery.
Symbol Digits Modalities Test (SDMT; Smith,
1982): It primarily assesses complex scanning and
visual tracking.
Verbal Fluency: Two verbal fluency tasks:
Animal Recall and Words from the letter F
were implemented, modified from the Controlled

1027

Oral Word Association Test (COWAT; Kosmidis,

Vlahou, Panagiotaki, & Kiosseoglou, 2004).
Verbal episodic memory tests
Greek version of the Logical Memory Story
A from the Wechsler Memory ScaleRevised:
Immediate and delayed recall of a short story material (Constantinidou & Ioannou, 2008; Wechsler,
1997).
Greek version of the Hopkins Verbal Learning
TestRevised
(HVLT:
Benedict,
Schretlen,
Groninger, & Brandt, 1998; adapted in Greek
by Constantinidou upon permission from
the publisher); Learning trials (first trial:
HVLT1 and the total score of the three learning trials: HVLTimmediate), delayed recall
(HVLTdelayed), to assess list learning and delayed
recall performance.
Vocabulary
The total number of correct responses in the
Greek Version of the Peabody Picture Vocabulary
Test (PPVTIII; Simos, Kasselimis, & Mouzaki,
2011) to assess receptive or passive vocabulary.
Reading measure
The total number of pseudowords read correctly
in 45 s as measured by a test of pseudowords in
Greek (Simos, Sideridis, Kasselimis, & Mouzaki,
2013).

Definition of the latent constructs

Episodic memory was defined as a latent factor with five reflective observed-score indicators:
Hopkins Verbal Learning Test Trial 1 (HVLT1),
the total score of the HVLT three learning trials (HVLTimmediate), and the delayed recall score
(HVLTdelayed), Logical Memory immediate, and
Logical Memory delayed. These measures are commonly used for measuring verbal episodic memory
in adults in clinical settings, but also in research
studies and are considered to represent encoding
and retrieval capacities.
Executive function was also defined as a latent
factor with five reflective indicators: Trail Making A
(TMTA), Trail Making B (TMTB), Symbol Digits
Modalities Test, Verbal Fluency for semantic category, and phonemic verbal fluency. The above tasks
are speeded, mainly measuring attentional control
and set-shifting and verbal fluency ability (Fisk &
Sharp, 2004; Jurado & Rosselli, 2007).

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GIOGKARAKI, MICHAELIDES, CONSTANTINIDOU

Defining a CR latent construct is a task with

important challenges. Latent variable models allow
the formulation of a CR factor from a combination of observed variables. Years of education is a
demographic variable used as an indicator of prior
experience contributing to CR. We added two more
observed measures: receptive vocabulary and reading performance. Both measures introduce important information about the quality of education
(Manly, Jacobs, Touradji, Small, & Stern, 2002) and
could be used as estimates of premorbid cognitive
ability (Crawford, Deary, Starr, & Whalley, 2001).
Moreover, these observed variables do not represent
an important overlap between the cognitive reserve
construct and the studied cognitive domains.
The specification of CR as a reflective latent
construct faces some conceptual difficulties. Years
of education, for example, is a characteristic that
occurs early in life and captures the extent of
prior experience. Evidently, years of education cannot be conceptualized as an effect of CR; rather,
it could be thought of as a contributor of the
CR. Instead, specifying CR as a formative latent
compositethat is, that it is caused by the three
observed measuresis also problematic because
formative measurement models have identification
problems (Kline, 2006) and provide no information
for the validity of the hypothesized latent factor
(Borsboom, 2005; Jones et al., 2011). Our approach
was to consider years of education as a formative
indicator for CR and the vocabulary and reading
performance as effect indicators that reflect the
level of CR. CR is thus specified as a multiple
indicators multiple causes (MIMIC) factor.

Structural equation modeling

Two structural equation models (SEMs) were
evaluated:
1. To test the direct relationships between age
and the two latent variables of verbal episodic
memory and executive function (Figure 1);
2. To test the moderating effect of CR between
age and verbal episodic memory and executive
function (Figure 2).
Confirmatory factor analysis and structural
equation modeling analyses were conducted with
AMOS 20 (Arbuckle, 2011), and maximum likelihood estimation was applied on the covariance
matrix of the data. Model fit was evaluated with
the chi-square test, as well as the following approximate fit indices: Bentlers (1990) Comparative Fit
Index (CFI) an incremental fit index that measures

the relative improvement in the fit of the hypothesized model over a baseline model that assumes
independence among factors. The root mean square
error of approximation (RMSEA; Hu & Bentler,
1998; Steiger, 1990) is a parsimony-adjusted index
that quantifies badness of fit. The standardized root
mean square residual (SRMR; Hu & Bentler, 1999)
represents a measure of the difference between
observed and predicted correlation, which should
be close to zero for an adequate model fit.

RESULTS
The correlation coefficients between all the variables appear on Table 2. As expected, performance on cognitive tasks is inversely related to
age and positively related to years of education.
Intercorrelations among the variables measuring
executive function were medium to high and significant; the same was true for the variables measuring
verbal episodic memory.
As a first step, a confirmatory factor analysis
model was run with the two outcome latent variables. Executive function and episodic memory had
five reflective indicators each, and the two latent
variables were allowed to correlate as is demonstrated by several studies that we have already
mentioned (Crawford et al., 2000; Salthouse &
Ferrer-Caja, 2003; Stuss & Alexander, 2000). Fit
indices were adequate, 2 (30) = 69.089, p < .001,
CFI = .979, RMSEA = .059, SRMR = .053,1 and
all indicators load significantly on their respective
latent factors. As expected, the two latent constructs of episodic memory and executive function
were significantly correlated in the confirmatory
factor analysis model (r = .620, p < .001).
The first model of the relationship between age,
episodic memory, and executive function had an
adequate model fit, 2 (38) = 85.643, p < .001,
CFI = .976, RMSEA = .058, SRMR = .052.
The estimated coefficients reveal significant negative effects of age on both latent cognitive factors
(see Figure 1). The unstandardized coefficient of
age on episodic memory is 0.084 (SE = 0.011,

1 Two

error covariances were added in the verbal episodic

memory indicators between (a) Logical Memory immediate and
Logical Memory delayed, which can be explained by the fact that
the two scores are based on the same test, and (b) HVLT1 and
Logical Memory delayed possibly indicating a common underlying mechanism of encoding. Two error covariances were added
in the executive function indicators between (a) the TimeA and
TimeB observed measurements probably because both are forms
of the same test and (b) fluency category and phonemic fluency,
as they are both measures of verbal fluency ability.

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COGNITIVE RESERVE IN AGING

1029

Figure 1. Schematic representation of the first structural equation model. The first model illustrates the relationship of age with episodic
memory and executive function. HVLT = Hopkins Verbal Learning Test; HVLT1: the number of recalled words in the first trial;
HVLTimmediate: the total number of words immediately recalled in the three learning trials; HVLTdelayed: the number of words
recalled in the delayed recall trial; TMTA = Trail Making Test Part A; TMTB = Trail Making Test Part B; SDMT = Symbol Digit
Modalities Test.

p < .001) and on executive function is 0.557

(SE = 0.071, p < .001). The standardized estimates, 0.380 and 0.425, respectively, show that
these effects are roughly of the same magnitude and
more than a third of a standard deviation. Squared
multiple correlations are .180 for executive function
and .145 for episodic memory and suggest that a
small portion of their variance is explained by age.
The second model (Figure 2), which included CR
as moderator, had acceptable fit indices, 2 (68) =
204.959, p < .001, CFI = .945, RMSEA = .073,
SRMR = .075. The regression coefficients on
Table 3 indicate that age has significant negative
direct effects on the outcome variables; however,
unstandardized estimates are much smaller in the
second than in the first model, but still significant
at level .05. Moreover, with the introduction of CR,
the effects in the indirect paths are in the expected
direction: Age has a significant negative effect on
CR, while the CR has a large positive significant

effect on verbal episodic memory and a very large

positive effect on executive function. Squared multiple correlations are much larger in the second
model: .861 for executive function and .248 for verbal episodic memory, indicating that the addition
of cognitive reserve in the model has contributed in
explaining much more variance in the two outcome
variables.
Finally, after removing the direct paths of age
on the two cognitive latent variables, the fit is
significantly worse, 2 (70) = 227.088, p < .001,
CFI = .937, RMSEA = .077, SRMR = .078,
and squared multiple correlations are very high:
.888 for executive function and .255 for verbal
episodic memory. Overall, these results demonstrate a significant moderating role of the CR construct as defined using information about education
and observed verbal measures in the relationship
between age and executive function and episodic
memory.

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1030

GIOGKARAKI, MICHAELIDES, CONSTANTINIDOU

Figure 2. Schematic representation of the second structural equation model. The second model introduces the multiple indicators
multiple causes (MIMIC) cognitive reserve latent variable as a moderator between age and the two cognitive outcomes. Schematic
representation of the first structural equation model. The first model illustrates the relationship of age with episodic memory and executive function. HVLT = Hopkins Verbal Learning Test; HVLT1: the number of recalled words in the first trial; HVLTimmediate: the
total number of words immediately recalled in the three learning trials; HVLTdelayed: the number of words recalled in the delayed recall
trial; TMTA = Trail Making Test Part A; TMTB = Trail Making Test Part B; SDMT = Symbol Digit Modalities Test.

DISCUSSION
The contribution of this study is twofold: methodological and theoretical. First, even if similar CR
constructs have been proposed in the literature (e.g.,
Siedlecki et al., 2009), our proposed MIMIC model
could be considered as a possible solution to the
methodological problem of using formative versus
reflective models in the definition of CR. Second,
the proposed CR construct has a moderating role
in reducing the direct effect of age in executive
functions and episodic memory, thus contributing
to the growing body of literature exploring the

potential role of CR on cognitive performance in

older adults.
We developed a MIMIC latent construct of CR
using three variables: years of education, receptive vocabulary, and reading ability. We propose
a simple construct of cognitive reserve based on
theoretical evidence and practical for large-scale
studies using variables that can be included as part
of a general population screening protocol. The
variable years of education is the most commonly
used measure for cognitive reserve and functions
as a formative indicator for CR. Years of education is considered to represent prior experience,

COGNITIVE RESERVE IN AGING

1031

TABLE 2
Pearson correlation coefficients among the study variables

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1. Age (years)
.210 .225 .092 .323 .349 .336 .145 .147
2. Education
.535 .312 .357 .330 .297 .333 .329
(years)
3. Vocabulary
.310 .256 .207 .316 .302 .299
4. Reading
.190 .189 .184 .137
.117
5. HVLT1
.799 .561 .436 .413
6. HVLTimmediate
.666 .488 .483
7. HVLTdelayed
.433 .531
8. LMimmediate
.723
9. LMdelayed
10. TMTA
11. TMT B
12. SDMT
13. Fluency
category
14. Phonemic
fluency

10

11

12

13

14

.316 .321 .372 .146 .177

.352 .431 .661 .356 .360
.423
.224
.362
.402
.286
.242
.260

.492 .566 .429 .299

.321 .271 .091
.178
.429 .381 .273 .314
.440 .423 .336 .382
.405 .416 .320 .313
.307 .379 .318 .256
.311 .373 .339 .264
.730 .587 .314 .285
.648 .391 .353
.424 .417
.409

Note. Vocabulary: number of correct responses in the Greek version of the Peabody Picture Vocabulary Test (PPVTIII; Simos et al.,
2011); Reading: the number of total pseudowords read correctly in 45 s (Simos et al., 2013); HVLT: Greek version of the Hopkins Verbal
Learning TestRevised (Benedict et al., 1998; adapted in Greek by Constantinidou upon permission from the publisher); HVLT1: the
number of recalled words in the first trial; HVLTimmediate: the total number of words immediately recalled in the three learning trials;
HVLTdelayed: the number of words recalled in the delayed recall trial; LM: Story A of Logical Memory subtest from Wechsler Memory
ScaleRevised (Wechsler, 1997); LMimmediate: the score in the immediate recall; LMdelayed: the score in the delayed recall; TMT: Trail
Making Test; TMTA: time in seconds for the TMT Part A; TMTB: time in seconds for the TMT Part B; SDMT: the correct responses
in 90 s in the Symbol Digit Modalities Test (Smith, 1982); Fluency category: the number of the correct words generated in 60 s for the
category animals; Phonemic fluency: the number of correct words starting with the letter F generated in 60 s.
p < .05. p < .01.
TABLE 3
Estimates of the unstandardized and standardized estimates of regression weights of the SEM models

Models
Structural Equation Model 1 (effect of
age on cognitive outcomes)
Structural Equation Model 2 (cognitive
reserve as moderator)

Age VEM
Age EF
Age VEM
Age EF
Age CR
CR VEM
CR EF

Unstandardized
estimates

Standard
error

Standardized
estimates

0.084
0.557
0.059
0.215
0.121
0.105
1.498

0.011
0.071
0.011
0.071
0.046
0.018
0.124

0.380
0.425
0.270
0.162
0.153
0.379
0.889

<.001
<.001
<.001
.002
.008
<.001
<.001

Note. SEM = structural equation modeling; VEM: the latent variable reflecting verbal episodic memory; EF: the latent variable reflecting
executive function; CR: the latent variable reflecting cognitive reserve.

which is contributing to CR. In this study, we have

been able to capture the last generation of Cypriots
who have attended very little formal schooling and
therefore study the effects of education in respect
to aging and cognition. We stress that this is the
last generation of individuals with very low education, because since the independence of Cyprus
and the establishment of the Republic of Cyprus in
1960, public education has been free and mandatory through Grade 9 (Cyprus Statistical Service,
2009). Prior to 1960, it was standard practice to
attend a few years of elementary school education
and then enter the work force. It is possible that

years of education might reflect cognitive potential

to some extent; however, in pre-1960 Cyprus, various socioeconomic factors such as poverty, social
status, gender, and place of birth dictated education
choices. We also added two measures as reflective
indicators (receptive vocabulary and reading ability), which introduce important information about
the quality of education (Manly et al., 2002) and
could be used as estimates of premorbid cognitive
ability (Crawford et al., 2001). Additionally, there is
not an important overlap between the outcome cognitive domains and the cognitive reserve construct.
This study reinforces the repeated observation that

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1032

GIOGKARAKI, MICHAELIDES, CONSTANTINIDOU

educational experience has a strong influence on

cognitive processing, and, therefore, educational
attainment, receptive vocabulary, and reading level
are good proxies for cognitive reserve (Stern, 2011).
Furthermore, we tested two SEM models.
We used SEM to test our hypothesis as it is considered a powerful statistical tool for analyzing
multivariate data in studies of neurobiology and
aging. We developed a parsimonious model, containing only the most relevant associations, which
are more likely to be generalizable (Penke & Deary,
2010).
The first model shows an expected negative effect
of age on both verbal episodic memory and executive function. The effect seems to be of the same
magnitude, showing that both of these cognitive
domains account for age-related changes in cognition. The second model assessed the moderating
role of CR. Findings reveal that CR moderates the
direct negative effect of aging in cognitive aging and
especially on executive function, in accordance with
the CR hypothesis. Both models have adequate fit.
Additionally, executive function and verbal
episodic memory are correlated. Therefore, we
could suppose a common underlying mechanism
that could interfere with CR. Several aspects of
executive function have indirect impact on memory: the organization and elaboration of material
of encoding, strategic retrieval of information, and
the ability to avoid the effects of interference (Stuss
& Alexander, 2000). If we take into account the
theoretical framework proposing that CR generates new cognitive strategies (Stern, 2002), strategy
thinking could be considered as the common underlying mechanism between executive function and
episodic memory. Our findings are in agreement
with a recent study that demonstrated that the
association between markers of reserve and cognition was weakest for the measure of memory
and strongest for the measure of reasoning (SinghManoux et al., 2011). In other words, adults with
higher levels of CR apply more elaborate learning and cognitive strategies, which may be more
relevant for reasoning and executive function and
more indirectly related to memory performance,
and this could probably explain why in the second
model we observe a stronger indirect effect of cognitive reserve on executive function than in verbal
episodic memory.
However, the present study has several limitations that should be noted. First, we did not
include brain measures (e.g., imaging). Therefore,
we could not evaluate the relationship of CR to
brain reserve and how these two constructs interact. Additionally, we included in our study a few
participants with low or even zero years of formal

education and consequently very low scores in

some neuropsychological measures. However, they
met our inclusion/exclusion criteria as their performance was within the expected ranges (for their
education levels), and they had no subjective complaints of memory or other cognitive impairments.
Future studies may decide to exclude participants
with the aforementioned profile.
Several latent variable models of reserve have
appeared in the scientific literature. Satz et al.
(2011) used the executive function construct as a
candidate measure of cognitive reserve. A robust
overlap seems to exist between a construct of
executive function and a construct of cognitive
reserve as lifetime experiences (Siedlecki et al.,
2009). However, certain aspects of executive function are linked to the prefrontal cortex, an area
that develops last during normal development and
at the same time is very vulnerable to age-related
degeneration (Raz, 2000). This degeneration of the
prefrontal cortex may lead to early decline in several
executive abilities (West, 1996). Thus, in accordance
with the gain/loss hypothesis, one should carefully
select aspects of executive function that are robust
and resistant to aging in order to include them
in future CR theoretical frameworks. Otherwise,
the executive function construct as defined in the
present study may not be an appropriate measure
for cognitive reserve since it is not stable across the
lifespan, and it is vulnerable to the changes associated with aging. Hence it could not have a dual
role, as a dependent measure of the impact of aging
(or pathology) and as a factor that modifies this
relationship.
Another construct, general intelligence (g), has
been reported as an important construct of cognitive reserve. Unlike crystallized or fluid intelligence (when adjusted for g), the construct g is
strongly linked to intracranial and brain volume,
especially prefrontal volume (Christensen, Anstey,
Leach, & Mackinnon, 2008). General intelligence,
unlike fluid ability, is also stable across the lifespan and is associated with cognition, education,
occupation, mental activities, and survival (Staff,
Murray, Deary, & Whalley, 2004; Sternberg, 2008).
However, there is also an overlap between the measures of cognitive performance and the estimation
of general intelligence.
A recent alternative approach to the measure
of cognitive reserve consists of decomposing the
variance in cognitive function scores (Reed et al.,
2010) and defining CR as a prediction score that
can be modified across time. Specifically, Reed and
colleagues described CR as a measure of episodic
memory adjusted for the effect of magnetic resonance imaging (MRI) and demographics (Reed

Downloaded by [187.141.45.19] at 12:11 21 August 2014

COGNITIVE RESERVE IN AGING

et al., 2010). This approach, while interesting and

innovative, it is not practical for large-scale studies since MRI findings are not routinely included
as part of a general population screening protocol.
Interestingly, Reed et al. (2011) showed that engaging in leisure cognitive activities at 40 and in late
life was the strongest predictor of cognitive reserve,
compared to socioeconomic status and education.
We plan to include cognitive leisure activities in our
future studies aiming at defining CR.
Future studies should also explore the potential effect of neurocognitive training in improving
or expanding CR. Recent clinical trials seem to
indicate that cognitive training can have a positive protective effect on longitudinal cognitive
change in both normative and preclinical groups
(Derwinger, Stitgsdotter Neely, & Backman, 2005;
Oswald, Gunzelamann, Rupprecht, & Hagen, 2006;
Valenzuela, 2008). The benefits are apparent not
only for the trained cognitive domains, but also for
the functionality of older adults in daily activities
(Valenzuela, 2008; Willis et al., 2006). It remains a
question whether people with higher reserve may
benefit more from cognitive training or cognitive
training may offer an opportunity for those with
low cognitive reserve to build one.
Cognitive aging is a heterogeneous and highly
individualized and complex process. The present
findings support the CR hypothesis and its moderating role in the relationships between chronological age and verbal episodic memory and executive function. The proposed MIMIC latent variable
offers a parsimonious and practical model of CR,
which can be easily implemented in large-scale studies on cognitive aging. Additionally, our proposed
model allows room for further development and
future expansion in order to eventually develop an
accurate and representation of reality. Specifically,
we plan to explore the contribution of biological
markers, such as cardiovascular health and genetic
factors (apolipoprotein E, ApoE) and indexes of
daily activities (cognitive, physical, and social) in
our proposed model on aging. We believe that this
approach will contribute to our understanding of
CR on healthy aging with important implications
on cognitive decline associated with the biological
aging.

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