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APPLIED NEUROPSYCHOLOGY: ADULT

2020, VOL. 27, NO. 6, 525–531


https://doi.org/10.1080/23279095.2019.1575219

WAIS Information Subtest as an indicator of crystallized cognitive abilities


and brain reserve among highly educated older adults: A three-year
longitudinal study
Odelia Elkanaa, Shani Soffera, Osnat Reichman Eisikovitsa, Noga Orenb,c,d, Vered Bezalelb, and
Elissa L. Ashb,d
a
Behavioral Sciences, Academic College of Tel Aviv-Yaffo, Yaffo, Israel; bDepartment of Neurology, Sourasky Medical Center, Tel Aviv,
Israel; cFunctional Brain Center, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel; dSackler
Faculty of Medicine, Tel-Aviv University, Tel Aviv, Israel

ABSTRACT KEYWORDS
The Wechsler Adult Intelligence Scale-Third Edition (WAIS-III) Information Subtest (IS) is Brain reserve; cognitive
known as a neuropsychological “Hold” test that is relatively resistant to decline with aging. decline; cognitive reserve;
We administered neuropsychological tests among highly educated healthy older adults elderly; high education;
information subtest; MRI;
once a year for three subsequent years. Results showed highly stable performances on the neuropsychological testing
IS across years (Mean Z score: T0 ¼ 1.39, SD ¼ 0.60; T1 ¼ 1.37, SD ¼ 0.77; T2 ¼ 1.50, SD ¼ 0.66;
T3 ¼ 1.48, SD ¼ 0.66), that were significantly higher than zero (T0: t ¼ 12.08; T1: t ¼ 9.29; T2:
t ¼ 11.71; T3: t ¼ 11.68; for all, p < 0.0001). In contrast, other neuropsychological tests
showed differences in performance across time; some performances significantly declined
(Rey Osterrieth Complex Figure test-copy, Rey-Auditory Verbal Learning Test, and Montreal
Cognitive Assessment test [MoCA]), whereas others were improved, possibly due to practice
effects (Rey Osterrieth Complex Figure test- delayed, Rey-Auditory Verbal Learning Test-
delayed, and Trail Making Test- part A). Correlation with whole brain volumetric analysis
revealed a positive correlation between gray matter volumes and IS scores (r ¼ 0.46,
p < 0.05) even when controlling for age and education (partial correlations: r ¼ 0.43; r ¼ 0.45,
for both p < 0.05). No significant correlations were found between gray matter and other
test scores. Therefore, the WAIS-III Information subtest appears to be an adequate neuro-
psychological measurement of crystallized ability in highly educated older adults and may
be considered as a proxy measure of brain reserve.

Introduction
crystalized (“Hold”) cognitive measures, extrapolation
The need for accurate and effective estimation of cog- from current abilities, demographic variables, or some
nitive ability has become increasingly apparent, espe- combination of these (Lezak, Howieson, Loring, &
cially when testing for possible mental deterioration in Fischer, 2012). Verbal skills are considered to be best
older individuals. Neuropsychological measures have preserved and relatively unaffected, long after recent
historically been used to assess cognitive decline as memory, reasoning, arithmetic ability, and other func-
well as to estimate premorbid abilities (Apolinario tions are severely compromised (Ryan, Sattler, &
et al., 2013). The assessment of cognitive decline is Lopez, 2000). Therefore, it is assumed that cognitive
made by comparison to premorbid ability as well as skills based on semantic knowledge acquired before
to normative data with similar demographics, particu- neurological damage are less affected and remain gen-
larly age, due to the expected decline associated with erally preserved. The discrepancy between performance
age (Elkana et al., 2016). on “Hold” tests and performance on other neurocogni-
Since most patients do not have documented records tive tests helps to assess and quantify the extent of cog-
of previous functioning, estimates of premorbid abilities nitive decline for a specific individual.
constitute a critical aspect of neuropsychological assess- The Information Subtest (IS) of the Wechsler Adult
ment. The common neuropsychological techniques Intelligence Scale-Third Edition (WAIS-III) is a widely
for estimating premorbid ability usually relies on used cognitive test for estimating premorbid ability

CONTACT Odelia Elkana odelia.elkana@gmail.com Academic College of Tel Aviv-Yaffo, 14 RabenuYerucham St. P.O. 8401, Yaffo, 68114, Israel.
ß 2019 Taylor & Francis Group, LLC
526 O. ELKANA ET AL.

Table 1. Participants’ characteristics.


Age (years) 72.6 (4.5) rang 66–80
Gender 12 Men/15 Female
Education (years) 17.14 (3.21) range: 12–24
BMI 26.7 (3.23) range: 20.5–32.5
Physical exercise: number of time on average 3 times a week
Leisure activity: number of times on average Between once to 3 times a week
Cognitive activity: number of weekly hours on average 1.5 h a week
Number of smokers 2
Country of birth Israel: 66.6%
Poland; Rumania: 7.4%
England; Egypt; Germany; Uzbekistan;
Argentina: 3.7%
Year of immigration in average 1956 (10.41) range (1948–1976)
Native language Hebrew: 70.3%
Yiddish: 11.1%
French; English; Hungarian; Russian; Spanish: 3.7%
All participants were fluent Hebrew speakers Fluent Hebrew- 100%
Country of parent’s Birth Poland: 48.1%
Israel: 18.5%
Rumania: 11.1%
Russia: 7.4%
Italy; Ukraine; Greece; England: 3.7%
Note. BMI ¼ weight (kg)  height2 (m2); SD = Standard Deviation.

level and is usually considered the best indicator of highly educated older adults are at high risk of being
original intellectual endowment (Ryan et al., 2000). under-diagnosed at the earliest stages of cognitive
Unlike other verbal tests, such as the vocabulary subt- decline (Elkana et al., 2016). These individuals, who
est, that require oral definition and tend to be more usually function far above the average norm from
vulnerable to brain damage, the IS can be answered in young adulthood, may experience subjective decline
a word or two and is thus more resistant to semantic with aging relative to their own baseline, while object-
losses. Moreover, the IS correlates strongly with edu- ively still perform within the age-matched norms
cation level, and usually serves as a good indicator of (Elkana et al., 2016). Although normative data strati-
premorbid ability (Tremont, Hoffman, Scott, & fied by age and education have been available, the
Adams, 1998). studies tend to focus on the effect of lower education,
A valid estimation of premorbid ability becomes whereas there is a relatively minimal amount of
crucial when individuals are located on either end of information regarding highly educated individuals
the education scale (highly educated and less edu- (O’Bryant et al., 2008). Therefore, in the present study
cated), where normative data is generally lacking
we wish to examine whether the IS reflects stable crys-
(Elkana et al., 2016). However, to the best of our
tallized ability in highly educated individuals, and if
knowledge, no study investigated the sensitivity of the
so, whether the performance on this test is positively
IS over time in highly educated, healthy adults.
correlated with gray matter brain volume. We
Higher education level is considered to serve as a
hypothesized that performances on the IS will be sta-
proxy for cognitive reserve (CR). Therefore, educated
ble over time (T0, T1, T2, T3), relative to more fluid
individuals are considered to have better tolerance for
brain damage due to greater cognitive reserve, cognitive abilities. In addition, we hypothesized that
reflected by generally preserved cognitive ability des- IS will positively correlate with whole brain gray
pite reduced brain volume (Arenaza-Urquijo, Wirth, matter volume (T0).
& Chetelat, 2015). Furthermore, higher levels of CR,
as assessed by educational level, have been found to
be associated with higher levels of brain reserve (BR), Materials and methods
such as brain volume (Arenaza-Urquijo et al., 2013). Participants
On one hand, a higher level of education could pro-
tect from cognitive loss and delay the overt expression Methods of this study were published elsewhere
of dementia due to higher CR (Apolinario et al., (Elkana et al., 2016). In short, at baseline, 28 healthy
2013). In this case, highly educated individuals have a elderly adults were recruited. After the first year, one
better capacity to compensate with normal or near participant was lost to follow up. Thus, the final sam-
normal cognitive functioning in the presence of vary- ple included 27 participants ages 66–80 (Mean ¼ 72.6,
ing amounts of brain damage. On the other hand, SD ¼ 4.5) with high educational level (see Table 1).
APPLIED NEUROPSYCHOLOGY: ADULT 527

Data collection and diagnosis were performed in matrix ¼ 256  256; TR ¼ 9.2 ms; TE ¼ 3.5 ms; axial
the Center for Memory and Attention Disorders and slices of 1 mm thickness, no gap.
Functional Brain Center, TASMC. Participants
received nominal financial compensation for their Neuropsychological Tests (for more detail, see
participation. Elkana et al., 2016)
Inclusion Criteria: (1) Men and women over the
age of 65; and (2) Men and women with flu-  Montreal Cognitive Assessment test (MoCA)
ent Hebrew. (Nasreddine et al., 2005): Screening test for MCI
Exclusion Criteria: (1) Diagnosis of cancer in the that estimates different cognitive functions, includ-
last five years (we wished to include participants with ing attentiveness and concentration, executive
stable health that can be followed for years); (2) functioning, memory, language, visuo-construc-
Existence of a neurological or psychiatric disorder; (3) tional ability, conceptual thinking, calculations, and
History of head injuries and/or head surgeries; (4) orientation.
The presence of metals implanted in their bodies or  Rey Auditory Verbal Learning Test (RAVLT)
tattoos (MRI prohibition); and (5) Claustrophobia. (Vakil & Blachstein, 1997): Provides an evaluation
None of the participants reported significant cogni- of verbal episodic memory that includes immediate
tive decline, and a board certified radiologist reviewed memory (Trial 1 and Trail 6), learning rate (Trial
all scans and found no significant lesions including 5 minus Trial 1), delayed memory (Trial 8), and
infarct, hemorrhage, or other brain lesions in any of recognition (Trial 9). In addition, the introduction
the subjects. of the interference list in Trial 6 (List B) enables
the extraction of two interference measures: pro-
active and retroactive interference. Proactive inter-
Procedure ference occurs when previously learned material
The institutional ethics committee approved the negatively affects the acquisition or recall of new
research and all participants signed informed consent. information. On the RAVLT it is expressed as
The participants attended a screening exam in which impaired learning of a new list (List B) after an
a highly structured clinical and neuropsychological earlier learning list (List A) (the measure: Trial 1
evaluation was administered (T0). minus Trial 6). Retroactive interference occurs
A brain MRI scan was conducted in a timeframe of when subsequent material (List B) negatively
a few weeks after the first meeting (Mean 33 days). affects the recall of previously learned material
Approximately 1 year after administration of the (List A). On the RAVLT it is measured by the
cognitive assessment (T0), participants were invited recall of List A after learning the distractor list
for follow-up assessments. Cognitive assessments iden- (List B) (the measure: Trial 5 minus Trial 7)
tical to those obtained at T0 were repeated at yearly (Vakil, Greenstein, & Blachstein, 2010).
intervals: T1 (1 year after the initial assessment), T2  Rey Osterrieth Complex Figure test (ROCF)
(2 years after the initial assessment), and T3 (3 years (Osterrieth, 1944): Measures visuospatial, episodic
after the initial assessment). In addition, a depression nonverbal memory, attention, planning, working
screening was performed, using the Beck Depression memory, delayed memory, coordination, and graph
motor abilities. The test consists of two-test condi-
Inventory questionnaire (BDI) due to the possible
tions: copy and delayed recall.
impact of depression on individual’s cognitive
performance (Beck, Ward, Mendelson, Mock, & The copy part involves mainly visual-constructional
Erbaugh, 1961). and executive function abilities (specially planning
and organizing skills) and the delayed part involves
mainly nonverbal memory.
Assessments
MRI data acquisition  Wechsler Adult Intelligence Scale (WAIS-III)
Information Subtest (IS) (Wechsler, 1997):
 MRI scans were performed on a 3.0 Tesla MRI Includes questions of general knowledge. This test
scanner (GE Signa EXCITE, Milwaukee, WI, USA) expressed so-called “Crystallized intelligence,” and
using an eight channel head coil. A high-resolution is thought to represent premorbid abilities, which
anatomical T1-weighted fast spoiled gradient often remain intact even in the face of major
echo image was acquired: FOV ¼ 256 mm; brain damage.
528 O. ELKANA ET AL.

 WAIS-III Digit Span Forward and Backward 2012). The association between brain volume and per-
Subtest (Wechsler, 1997): Provides evaluation of formance on the IS was calculated using Pearson cor-
verbal attention and working memory. relations. Repeated measures ANOVA were performed
 Trail Making Test (TMT), Parts A and B (Army with TIME (T0/T1/T2/T3) as the within-subject vari-
Individual Test Battery, 1944): provides informa- able. A post hoc test (Bonferroni) was used to correct
tion of visual search, attention, speed processing, for multiple comparisons to identify the significant
mental flexibility, and executive functions. The differences among the years.
TMT consists of two parts. Part A is considered a
measure of visual search and mental tracking,
whereas Part B is assumed to encompass cognitive
abilities such as flexibility, to shift the course of an
Results
ongoing activity and the capacity to deal with Cognitive differences between the four testing
more than one stimulus at a time (Fernandez & examinations
Marcopulos, 2008).
There were no significant differences between per-
 Verbal Fluency Test: Phonetic Fluency (PF) and
formances on the IS across examinations [Mean Z
Semantic Fluency (SF) (Kave & Knafo-Noam,
score: T0 ¼ 1.39 (0.60); T1 ¼ 1.37 (0.77); T2 ¼ 1.50
2015): Examines retrieval of words, initiation and
(0.66); T3 ¼ 1.48 (0.66)].
mental flexibility. The test includes two parts; (1)
On other tests, significant decline across TIME was
Phonemic Fluency (PF): letters Bet, Gimel, & Shin
found in the ROCF-copy [F(3,78) ¼ 4.09, p < 0.01,
in Hebrew; and (2) Semantic Fluency (SF): ani-
partial ¼ 0.13]; MOCA [F(3,78) ¼ 3.90, p < 0.05, parti-
mals, fruits, & vegetables.
 BDI (Beck et al., 1961): One of the most common al ¼ 0.13)]; and the RAVLT- proactive interference
tools for measuring the severity of depression. The [F(3,78)= 3.21, p < 0.05, partial ¼ 0.18].
BDI consists of a list of descriptive statements On the contrary, significant improvement across
related to 21 aspects of depression. For each cat- TIME was observed for the RAVLT-8 [F(3,78) ¼ 2.67,
egory, there are four to five statements of increas- p < 0.05, partial ¼ 0.10]; RAVLT-9 [F(3,78) ¼ 3.35,
ing severity. The participant reads the scale and p < 0.05, partial ¼ 0.11]; ROCF-delay [F(3,78)= 2.93,
marks the statement most applicable to himself. p < 0.05, partial ¼ 0.10]; and the Trail Making test
The score for each item ranges from 0 to 3; the (part A) [F(3,78) ¼ 10.39, p < 0.01, partial ¼ 0.28]
total score falls between 0 and 62 (Salkind, 1969). (Table 2).
Internal consistency for the BDI ranges from .73 to Importantly, the observed changes in cognitive per-
.92 with a mean of .86 (Beck, Steer, & Carbin, formances were not likely due to mood changes, as
1988). In the present study, the internal consist- the participants were not depressed and there was no
ency was 0.79. significant effect of TIME on BDI scores.

Data analysis
Correlation of neuropsychological tests and
A whole-brain, voxel-based morphometry analysis was brain volume
conducted via Brain Voyager software (Goebel,
Esposito, & Formisano, 2006), using standard proce- We found a significant positive correlation between
dures (Brain Voyager). Gray matter volume was calcu- gray matter percentage and IS score (at all four
lated as a percentage from all brain matter as follows: examinations) (T0: r ¼ 0.45, p < 0.05), meaning that
Gray matter/(Gray Matter þ White Matter þ Lateral individuals with a larger percentage of gray matter
Ventricles). For more details, see Elkana et al. (2016). performed better on the IS and vice versa
Statistical analyses were performed using SPSS21 (Figure 1-T0).
software. All tests, except the MoCA, were scored This correlation was still significant after control-
using norms for age. These standardized scores ling for age and education as possible confounders
allowed comparison of different tests and examination [partial correlation – age (T0): r ¼ 0.43; education
within subject variance. A descriptive statistical ana- (T0): r ¼ 0.45, for both p < 0.05]. No other significant
lysis of the characteristics of the sample was then con- correlations were found between gray matter percent-
ducted. For the MoCA test, raw scores were used age volume and other neuropsychological
since there are no formal norms for age (Lezak et al., tests (p > 0.05).
APPLIED NEUROPSYCHOLOGY: ADULT 529

Table 2. Differences in cognitive performance between the four testing sessions T0–T3.
T0 T1 T2 T3 Repeated measures
Test/Questionnaire Z score (SD) Z score (SD) Z Score (SD) Z Score (SD) ANOVA F score (p)
RAVLT-1 0.13 (0.74) 0.04 (0.74) 0.27 (1.10) 0.35 (1.06) 1.57 (0.20)
RAVLT-5 0.06 (0.89) 0.07 (0.99) 0.07 (0.97) 0.19 (0.88) 0.42 (0.73)
RAVLT-6 0.39 (1.32) 0.25 (1.09) 0.04 (0.93) 0.12 (0.94) 1.83 (0.14)
RAVLT-7 0.17 (0.97) 0.01 (1.20) 0.27 (0.97) 0.37 (0.91) 2.53 (0.06)
RAVLT-8 0.38 (1.23) 0.29 (1.25) 0.11 (1.13) 0.23 (1.05) 2.67 (0.04)
RAVLT-9 0.04 (0.73) 0.03 (0.87) 0.38 (0.75) 0.43 (0.72) 3.35 (0.02)
Proactive Interference 0.50 (1.24) 0.23 (1.00) 0.17 (1.08) 0.20 (1.04) 3.21 (0.02)
Retroactive Interference 0.16 (1.05) 0.08 (0.99) 0.28 (0.96) 0.32 (0.94) 2.22 (0.09)
Total learning 0.02 (0.91) 0.10 (0.99) 0.36 (1.02) 0.49 (0.93) 2.20 (0.09)
ROCF-copy 1.29 (0.50) 0.81 (0.54) 0.85 (0.68) 0.92 (0.65) 4.09 (0.00)
ROCF-delayed 0.57 (0.75) 0.71 (0.84) 1.04 (0.85) 1.13 (0.88) 2.93 (0.03)
PF 0.28 (0.98) 0.34 (0.99) 0.51 (0.85) 0.40 (0.98) 0.44 (0.72)
SF 0.64 (1.11) 0.53 (1.04) 0.51 (1.20) 0.56 (1.06) 0.14 (0.93)
WAIS – digit span 0.14 (0.98) 0.26 (0.86) 0.09 (1.07) 0.09 (1.07) 0.38 (0.76)
TMT – A 0.01 (0.57) 0.16 (0.66) 0.43 (0.71) 0.71 (0.58) 10.39 (0.00)
TMT – B 0.63 (0.54) 0.66 (0.55) 0.84 (0.44) 0.84 (0.44) 1.51 (0.21)
IS 1.39 (0.60) 1.37 (0.77) 1.50 (0.66) 1.48 (0.66) 0.49 (0.68)
MoCA (raw score) 26.55 (1.50) 25.85 (1.45) 25.00 (2.16) 25.88 (1.94) 3.90 (0.01)
BDI (raw score) 4.70 (3.99) 5.81 (5.06) 6.55 (4.00) 5.48 (4.26) 1.18 (0.32)
Note. RAVLT ¼ Rey Auditory Verbal Learning Test; Proactive Interference ¼ Trial 1 minus Trial 6; Retroactive Interference ¼ Trial 5 minus Trial 7; Total
learning ¼ Sum of Trials 1 through 5; ROCF ¼ Rey Osterrieth Complex Figure test; PF ¼ Phonetic Fluency; SF ¼ Semantic Fluency; TMT ¼ Trail Making
Test Parts A and B; IS ¼ Information Subtest of WAIS-III; MoCa ¼ Montreal Cognitive Assessment test; BDI ¼ Beck Depression Inventory.
p < 0.05. p < 0.01.

Figure 1. Pearson Correlation: Percentage (%) gray matter and information subset.

Discussion based on executive functions are more sensitive for


detecting subtle cognitive changes.
In the present study we wished to examine whether the Interestingly, performance on certain tests improved
IS of the WAIS-III reflected stable crystallized ability in between the first and the fourth examinations (ROCF-
highly educated individuals, and if so, whether their delay, RAVLT- Trials 8 & 9 and TMT- Part A). This
performance on this test was positively correlated with improvement would be commonly viewed as a practice
gray matter brain volume. Our two hypotheses were effect, which derives from repeated exposure to the test
confirmed. First, our results demonstrate that in our materials (Duff, Callister, Dennett, & Tometich, 2012).
group, performance on the IS was stable across time However, practice effects may result from different fac-
while other performances significantly decreased, albeit tors such as memory for specific test items, learned
still within the “normal range.” This latter intriguing strategies, or test sophistication (Calamia, Markon, &
finding is discussed at length in Elkana et al. (2016). Tranel, 2012). These factors can be divided into two
Our findings strengthen the sensitivity of the ROCF- major components, familiarity with the task setup or
copy and RAVLT, by showing persistent decline even task demands, and familiarity with specific items, such
in a three-year follow-up, suggesting that tests that are as words on a list or a story to be recalled (Goldberg,
530 O. ELKANA ET AL.

Harvey, Wesnes, Snyder, & Schneider, 2015). In the A few limitations should be mentioned. The sample
present study, improvement was found in tests which size was relatively small, and it will be important to
included a delayed part; the participants were already confirm these results in a larger sample of older
familiar with the sequence of the tests and their expect- highly educated adults.
ation of the delayed part might have led them to better In addition, we used the Information subtest of the
performance. In line with these results, Beglinger et al. WAIS-III. This is because, unfortunately, that is the
(2005) investigated the practice effect and showed sig- latest version (Adapted to Hebrew speakers) available
nificant improvement on a wide range of neuropsycho- in Israel. The WAIS-III Information subtest is not
logical tests. Similarly, several studies have found identical to the latest Information subtest of the
practice effects to persist years after testing (R€onnlund, WAIS-IV (26 instead of 28 items, with 15 retained
Nyberg, B€ackman, & Nilsson, 2005; Van der Elst et al., and 11 new items, discontinue criterion, and revised
2008), even after 7 years (Salthouse, Schroeder, & scoring). However, the information subtests of the
Ferrer, 2004). These findings support and reinforce the WAIS-III and of the WAIS-IV seem to have the same
practice effect found in our study. Moreover, studies structural configuration and appear to measure similar
showed that both higher IQ and greater education are constructs (Taub & Benson, 2013). Therefore, we
associated with larger practice effects on some tests assume that the same patterns would emerge with the
such as the TMT (Calamia et al., 2012), similar to our WAIS-IV. Future longitudinal studies should also
finding regarding highly educated elders. Future combine computerized neuropsychological measure-
research should therefore investigate whether improve- ments such as processing speed and include a com-
ment on certain tests could indirectly indicate higher parison to a more heterogeneous group of individuals
CR, reflecting adaptive mechanisms, which rapidly lead with a wider range of educational level.
to increased efficiency (Barulli & Stern, 2013).
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