Psychological Medicine, Page 1 of 8.

f Cambridge University Press 2012 O R I G I N A L AR T I C LE

doi:10.1017/S0033291712000451

The relationship between executive functions

and fluid intelligence in Parkinson’s disease

M. Roca1,2,3, F. Manes1,2, A. Chade1,2, E. Gleichgerrcht1, O. Gershanik2, G. G. Arévalo1,2, T. Torralva1,2

and J. Duncan4*
1
Institute of Cognitive Neurology (INECO), Buenos Aires, Argentina
2
Laboratory of Neuroscience, Universidad Diego Portales, Chile
3
Institute of Neurosciences Favaloro University, Buenos Aires, Argentina
4
MRC Cognition and Brain Sciences Unit, Cambridge, UK

Background. We recently demonstrated that decline in fluid intelligence is a substantial contributor to frontal
deficits. For some classical ‘ executive ’ tasks, such as the Wisconsin Card Sorting Test (WCST) and Verbal Fluency,
frontal deficits were entirely explained by fluid intelligence. However, on a second set of frontal tasks, deficits
remained even after statistically controlling for this factor. These tasks included tests of theory of mind and
multitasking. As frontal dysfunction is the most frequent cognitive deficit observed in early Parkinson’s disease (PD),
the present study aimed to determine the role of fluid intelligence in such deficits.

Method. We assessed patients with PD (n=32) and control subjects (n=22) with the aforementioned frontal tests
and with a test of fluid intelligence. Group performance was compared and fluid intelligence was introduced as a
covariate to determine its role in frontal deficits shown by PD patients.

Results. In line with our previous results, scores on the WCST and Verbal Fluency were closely linked to fluid
intelligence. Significant patient–control differences were eliminated or at least substantially reduced once fluid
intelligence was introduced as a covariate. However, for tasks of theory of mind and multitasking, deficits remained
even after fluid intelligence was statistically controlled.

Conclusions. The present results suggest that clinical assessment of neuropsychological deficits in PD should include
tests of fluid intelligence, together with one or more specific tasks that allow for the assessment of residual frontal
deficits associated with theory of mind and multitasking.

Received 19 July 2011 ; Revised 22 February 2012 ; Accepted 22 February 2012

Key words : Executive function, fluid intelligence, frontal lobe, Parkinson’s disease.

Introduction tests of processing speed (e.g. Nettelbeck, 1987), and

many more, suggest that g reflects cognitive functions
In 1904, Charles Spearman proposed the existence of a
of importance in any form of organized behavior.
general factor that contributes to all cognitive activities
Obvious candidates are the broad organizational
(Spearman 1904, 1927). Spearman’s general factor (g)
functions of the frontal lobe, and indeed, performance
was proposed to explain one of the strongest findings
in fluid intelligence tests is impaired after frontal lobe
in the study of human intelligence – the universal
lesions, in particular lesions in lateral and dorsomedial
positive correlations typically found between different
frontal regions (Duncan et al. 1995 ; Woolgar et al. 2010).
cognitive tests. The best measures of g are generally
Similar regions are active in functional imaging studies
tests of so-called fluid intelligence, involving novel
of fluid intelligence test performance (Prabhakaran
problem-solving (Carroll, 1993). The cognitive func-
et al. 1997 ; Esposito et al. 1999 ; Duncan et al. 2000 ;
tions reflected in g are still under active study. Positive
Bishop et al. 2008).
g correlations for all manner of cognitive tasks, in-
Many clinical and experimental tests are known to
cluding tests of working memory, especially working
be sensitive to frontal impairment, even if they are
memory for novel task rules (Duncan et al., in press),
also known to recruit other cognitive functions and
brain areas. The Wisconsin Card Sorting Test (WCST)
* Address for correspondence : Dr J. Duncan, MRC Cognition and
and Verbal Fluency, for example, are often used to
Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 7EF, UK. measure frontal ‘ executive ’ impairment, even though
(Email : john.duncan@mrc-cbu.cam.ac.uk) both certainly also involve a variety of posterior
The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons
Attribution-NonCommercial-ShareAlike licence <http://creativecommons.org/licenses/by-nc-sa/2.5/>. The written permission of
Cambridge University Press must be obtained for commercial re-use.
2 M. Roca et al.

cortical functions. Recent attention has also been given Method

to tests of multitasking (e.g. Manly et al. 2002) and
Participants
theory of mind (e.g. Stone et al. 1998), although again,
it is likely that individual tests have contributions Thirty-two patients who met the UK Parkinson’s
from both frontal and posterior functions. Disease Society Brain Bank criteria, between Hoehn
The importance of the frontal lobe in fluid intelli- and Yahr stages I–III (Hoehn & Yahr, 1967), were re-
gence and in a diversity of specific cognitive tests cruited from the INECO Data Base in Buenos Aires,
raises the question of how much a loss of fluid intelli- Argentina and from the Movement Disorders Clinic
gence contributes to other frontal deficits. In a recent at the Institute of Neuroscience of the Favaloro
study (Roca et al. 2010a), we showed that, in a group Foundation. Mean (¡S.D.) age for the patient popu-
of patients with frontal lesions, fluid intelligence (g) lation was 62.25 (¡10.23) years. Information on dis-
was a substantial contributor to many frontal deficits. ease history and drug therapy was obtained by
For some classical ‘ executive ’ tasks, such as the WCST neurologists specialized in studying PD (A.C., G.G.A.,
and Verbal Fluency, frontal deficits were entirely O.G.). Patients with different neurological diagnoses
explained by individual scores of g. Once fluid intelli- or presenting radiological structural brain abnormali-
gence was partialled out, there was no remaining ties compatible with diagnoses other than PD were
difference between patients and normal controls. excluded from this study. Patients who scored under
However, on a second set of frontal tasks, performance 24 on the Mini-Mental State Examination (Folstein
deficits remained even after fluid intelligence was et al. 1975) were also excluded to ensure a good level of
statistically controlled. Such tasks were associated overall cognitive functioning. Of the patients selected,
particularly with anterior frontal damage [Brodmann 15 were under pharmacological treatment with either
area (BA) 10] and included tests of theory of mind levodopa or a dopamine agonist with a mean levodopa
(Faux Pas) and multitasking (Hotel Task), among equivalent daily dose of 318.56 (¡268.48) mg. Among
others. those patients, assessment was conducted during the
Although Parkinson’s disease (PD) is characterized ‘ on ’ state of the medication. Seventeen of the patients
by its motor symptoms, it is now widely accepted were not taking any medication for their motor symp-
that cognitive changes can also be present, even dur- toms. Performance between medicated and non-medi-
ing the early stages of the disease. Most frequently, cated patients was compared to ensure that the results
cognitive deficits exhibited by PD patients resemble were not influenced by medication intake. For cases in
those produced after frontal-lobe damage, with par- which significant differences between medicated and
ticular difficulties on executive functioning (Foltynie non-medicated patients were found, the levodopa
et al. 2004 ; Lewis et al. 2005 ; Muslimovic et al. 2005 ; equivalent daily dose (mg) was introduced as a co-
Williams-Gray et al. 2007), theory of mind (Saltzman variable in subsequent analysis. Permission for the
et al. 2000 ; Mengelberg & Siegert, 2003 ; Mimura et al. study was initially obtained from the local research
2006 ; Perón et al. 2009 ; Bodden et al. 2010 ; Roca et al. ethics committee and all participants gave their signed
2010b) and multitasking (Perfetti et al. 2010). informed consent prior to inclusion. The subjects’
Fluid intelligence loss has also been described consent was obtained according to the Declaration of
in PD, most commonly as measured by Raven’s Helsinki.
Colored Progressive Matrices (RCPM ; Pillon et al. Healthy control volunteers (n=22) were recruited
1995 ; Bostantjopoulou et al. 2001 ; Basić et al. 2004 ; through word of mouth and were matched to patients,
Nagano-Saito et al. 2005). In PD patients, performance taking into account the mean and range of age and
in RCPM has been shown to correlate positively with level of education. Controls were recruited from the
gray matter density within the dorsolateral prefrontal same geographical area as patients. Participants were
cortex (Nagano-Saito et al. 2005). included in the control group if they reported no his-
Although both frontal deficits and fluid intelligence tory of neurological or psychiatric disorders, including
loss have been described in PD, to our knowledge traumatic brain injury or substance abuse.
no previous study has investigated the role of fluid Clinical and demographical data for all participants
intelligence in frontal deficits associated with this dis- are shown in Table 1.
ease. To achieve this objective, we assessed a group
of patients with PD using tasks sensitive to frontal
Procedure
dysfunction and with the RCPM as a test of fluid
intelligence. In addition to comparing PD patients All participants were initially assessed using a com-
with a group of controls, we investigated how far plete neuropsychological battery that included cogni-
frontal deficits in PD were explained by fluid intelli- tive screening tests, tests of language, memory, praxis,
gence loss. attention and executive functions and pre-morbid IQ.
 Fluid intelligence in Parkinson’s disease 3

Table 1. Clinical and demographical data categories achieved. Data were available for 31/32
patients.
PD Controls

Mean S.D. Mean S.D. p Verbal Fluency (Benton & Hamsher, 1976)

Age (years) 62.25 10.23 59.27 1.98 0.33 In verbal fluency tasks, the subject generates as many
Education (years) 13.91 4.80 14.5 2.79 0.57 items as possible from a given category in a specific
WAT-BA 36.91 4.36 38.68 2.93 0.10 period of time. We used the standard Argentinean
Hoehn & Yahr (1967) 1.46 5.82 – – phonemic version (Butman et al. 2000), asking subjects
Disease duration 1.47 1.46 – – to generate words beginning with the letter P in a
(years) 1-min block. The score was the total number of correct
words generated.
PD, Parkinson’s disease ; WAT-BA, Word Accentuation
Test – Buenos Aires ; S.D., standard deviation.

Hotel Task (Manly et al. 2002 ; Torralva et al. 2009)

Experimental tests were administered during a second
session of assessment, including both theory of mind The task comprised five primary activities related to
and multitasking tasks. running a hotel. Individual activities are described in
more detail elsewhere (Torralva et al. 2009 ; Roca et al.
2010a). Subjects were told to execute at least some of
Neuropsychological testing
all five activities during a 15-min period, so that, at
Word Accentuation Test – Buenos Aires (WAT-BA) the end of this period, they would be able to give an
estimate of how long each would take to complete. It
To estimate pre-morbid intelligence we used the
was explained that the time available was not enough
WAT-BA (Burin et al. 2000). This test, similar to the
to complete any of the tasks ; the goal, instead, was to
National Adult Reading Test (Nelson & Willison,
ensure that every task was attempted. Subjects were
1991), measures ability to read 44 irregularly stressed
also asked to remember to open and close the hotel
Spanish words. The score was the number of words
garage doors at particular times (open at 6 min, close
stressed correctly.
at 12 min), using an electronic button. The score was
time allocation : for each primary task we assumed an
RCPM
optimal allocation of 3 min, and measured the sum-
To assess fluid intelligence, we used the RCPM med total deviation (in seconds) from this optimum.
(Raven, 1995), which is a multiple-choice test of novel Total deviation was given a negative sign, so that high
problem-solving comprising 36 items. In each test scores meant better performance. Data were available
item, the subject is asked to identify the missing item for 29/32 patients.
that completes a certain pattern. The test is organized
in three sets of 12 items ranging in complexity (series
A, Ab and B). The score was the total number of items Faux Pas (Stone et al. 1998)
solved correctly.
On each trial of this test, the subject was read a short,
one-paragraph story. To reduce working memory
WCST (Nelson, 1976)
load, a written version of the story was also placed in
For the WCST, we used Nelson’s modified version of front of the subject. In 10 stories, there was a faux pas,
the standard procedure. Cards varying on three basic involving one person unintentionally saying some-
features (color, shape and number of items) must be thing hurtful or insulting to another. In the remaining
sorted according to each feature in turn. The partici- 10 stories, there was no faux pas. After each story, the
pants’ first sorting choice becomes the correct feature, subject was asked whether something inappropriate
and once a criterion of six consecutive correct sorts was said and, if so, why it was inappropriate. If the
is achieved, the subject is told that the rules have answer was incorrect, an additional memory question
changed, and cards must be sorted according to a was asked to check that basic facts of the story were
new feature. After all three features have been used retained ; if they were not, the story was re-examined
as sorting criteria, subjects must cycle through them and all questions repeated. The score was 1 point
again in the same order as they did before. Each time for each faux pas identified correctly, or non-faux
the feature is changed, the next must be discovered pas rejected correctly. Data were available for 31/32
by trial and error. The score was the total number of patients.
4 M. Roca et al.

Table 2. Patient and control scores, average within-group correlation with Raven Colored Progressive Matrices (RCPM), and
significance of group differences for each task

Average Patients versus

Patients Controls Patients within-group controls after
versus correlations adjustment for
Mean S.D. Mean S.D. controls p with RCPM RCPM p

RCPM 27.78 5.98 31.27 3.90 0.02 – –

WCST (categories 4.61 1.64 5.55 0.80 <0.01 0.70 0.34
achieved)
Verbal Fluencya 14.31 4.78 18.09 5.07 <0.01 0.43 0.07
Hotel Taskb x460.41 219.10 x300.91 142.10 <0.01 0.47 0.04
Faux Pas (max=20) 17.74 1.91 18.86 1.35 0.02 0.14 0.06
Mind in the Eyes 13.42 1.68 14.64 1.29 <0.01 0.11 0.02
(max=17)

WCST, Wisconsin Card Sorting Test ; S.D., standard deviation.

a
Total number of words generated.
b
Deviation from optimum time per task.

Mind in the Eyes (Baron-Cohen et al. 1997) Fluency. Analysis of covariance (ANCOVA) was used
to compare patients and controls, adjusting for the
This task consisted of 17 photographs of the eye region
difference in RCPM ; regression lines in Fig. 1 come
of different human faces. Participants were required
from this ANCOVA model, reflecting the average
to make a two-alternative forced choice that best
within-group association of the two variables and
described what the person was thinking or feeling
constrained to have the same slope across groups. As
(e.g. worried–calm). The score was the total number
calculated from the corresponding variance terms
correct. Data were available for 31/32 patients.
of the ANCOVA, average within-group correlations
with RCPM were 0.70 for WCST and 0.43 for Verbal
Fluency. The scatterplots suggest that, at least for the
Results
WCST, PD deficits were largely or entirely explained
The results are shown in Table 2. For all cognitive by fluid intelligence. The group effect was to shift the
tasks, two-tailed t tests were used to compare patients RCPM distribution downward, leaving its relationship
and controls. As expected, the PD group was sig- to executive task performance largely unchanged. In
nificantly impaired on all tests, including the RCPM line with this conclusion, for the WCST, the difference
[t(52)=x2.40, p=0.02], the classical executive tests between patients and controls was far from significant
[WCST : t(51)=x2.45, p<0.01 ; Verbal Fluency : once RCPM was introduce as a covariate (Table 2,
t(52)=x2.78, p<0.01] and the tests of multitasking p=0.34). For Verbal Fluency, ANCOVA showed a re-
and theory of mind [Hotel : t(49)=x2.97, p<0.01 ; maining but non-significant trend for a group differ-
Mind in the Eyes : t(51)=x2.83, p<0.01 ; Faux Pas : ence (p=0.07).
t(51)=x2.35, p=0.02]. No significant differences Scatterplots relating RCPM to the other frontal
were found between medicated and non-medicated tests are shown in Fig. 2. For the Hotel Task, the results
patients on any of the aforementioned variables, except were somewhat similar to those observed in Verbal
for the Faux Pas, on which medicated patients per- Fluency, with an average within-group correlation
formed more poorly than non-medicated patients of 0.47. However, using ANCOVA to remove the in-
[t(29)=x2.46, p=0.02]. However, significant differ- fluence of RCPM, the comparison between groups
ences between patients and controls persisted after the remained significant (Table 2, p<0.04). On the theory-
levodopa equivalent daily dose (mg) was introduced of-mind tasks, the scores were barely related to
as a covariable (p=0.03), suggesting that group differ- RCPM, with average within-group correlations of 0.14
ences were not related to medication intake. for Faux Pas and 0.11 for Mind in the Eyes. Using
Scatterplots relating RCPM to the two classical ANCOVA to remove the influence of RCPM, signifi-
frontal tests are shown in Fig. 1, revealing that higher cant group differences for Mind in the Eyes persisted
scores in the RCPM were strongly associated with (Table 2, p<0.02), whereas for Faux Pas, the difference
better performance on both the WCST and Verbal now fell just short of significance (p=0.06).
 Fluid intelligence in Parkinson’s disease 5

(a) (a)
WCST (number of categories achieved)

Hotel (deviation time in seconds)

6
–200
5
–400
4
–600
3
–800
2 Controls
Controls –1000 Patients
Patients
1
15 20 25 30 35
15 20 25 30 35 RCPM (total score)
RCPM (total score)

(b) (b)
30 20
Controls
19
Verbal fluency (total score)

Patients
25

Faux (total score)

18
20 17
16
15 Controls
15 Patients

10 14

5 13

15 20 25 30 35 15 20 25 30 35
RCPM (total score) RCPM (total score)

Fig. 1. Scatterplots relating performance in (a) the Wisconsin (c)

Card Sorting Test (WCST) and (b) Verbal Fluency to Raven’s 17
Controls
Mind in the eyes (total score)

Colored Progressive Matrices (RCPM) for patients with 16 Patients

Parkinson’s disease (PD) (circles) and controls (crosses).
15
Regression lines (broken for PD and solid for controls) reflect
the average within-group association of the two variables, as 14
determined by ANCOVA, constrained to have the same slope 13
across groups.
12
11
Discussion
10
In this study, we aimed to investigate the role of 15 20 25 30 35
fluid intelligence in different frontal deficits shown RCPM (total score)
in a group of patients with PD. In line with previous
Fig. 2. Scatterplots relating performance in (a) Hotel, (b) Faux
studies (Pillon et al. 1995 ; Bostantjopoulou et al.
Pas and (c) Mind in the Eyes to Raven’s Colored Progressive
2001 ; Basić et al. 2004 ; Nagano-Saito et al. 2005),
Matrices (RCPM) for patients with Parkinson’s disease (PD)
we found a loss of fluid intelligence in PD patients (circles) and controls (crosses). Regression lines (broken for
relative to control subjects. In the present study, PD and solid for controls) reflect the average within-group
this was found even in the absence of significant association of the two variables, as determined by ANCOVA,
differences between the groups on pre-morbid constrained to have the same slope across groups.
IQ. We then asked what other cognitive deficits re-
mained after statistical control for this fluid intelli-
gence deficit. These results are largely compatible with data from
For the classical executive tasks, WCST and Verbal patients with focal frontal lesions. In a recent study
Fluency, deficits in PD patients were no longer present (Roca et al. 2010a) we showed that for the WCST and
once g was introduced as a covariate. However, for Verbal Fluency deficits of frontal patients were en-
other tasks, including multitasking and theory-of- tirely explained by their fluid intelligence loss. The
mind tests, performance deficits remained once fluid present study extends those results to patients with
intelligence was partialled out. PD : even if original differences emerged when the PD
6 M. Roca et al.

group was compared with a group of control subjects, significance (p=0.34) once fluid intelligence was con-
such differences became non-significant when fluid trolled. The results are very similar to those we ob-
intelligence was introduced as a covariate. tained previously for patients with focal lesions
Our data also replicate previous reports of multi- (p=0.36). For Verbal Fluency the evidence of overlap
tasking and theory-of=mind deficits in patients with was less, with a marginal difference (p=0.07) remain-
PD. PD patients showed deficits in their ability to infer ing after fluid intelligence was controlled. Again this
other people’s thoughts and feelings (theory of mind) resembles our previous results (p=0.07). For multi-
and in their ability to hold in mind a higher-order goal tasking and theory of mind, overlap with fluid intelli-
while performing other subgoals (Hotel Task). Unlike gence may be weaker, although especially for
the findings for the WCST and Verbal Fluency, per- multitasking, some correlation certainly exists. For
formance deficits on the Hotel Task and Mind in the some tests, accordingly, fluid intelligence accounts for
Eyes remained significant even after fluid intelligence the major part of frontal deficit, whereas for others,
was statistically corrected. Again the results resemble probably with a somewhat different anatomical sub-
those obtained previously in patients with focal frontal strate, it does not.
lesions (Roca et al. 2010a). In that study also, we found Our data have strong implications for the use and
that deficits in multitasking and theory of mind were interpretation of executive tests such as the WCST and
not fully explained by fluid intelligence, with some Verbal Fluency in patients with PD. Although several
evidence of link to lesions in the anterior frontal cortex reports have highlighted the sensitivity of such tests
(BA 10). In the Roca et al. (2010 a) study, the theory-of- in the detection of cognitive dysfunction in PD (e.g.
mind test that showed these results was the Faux Green et al. 2002 ; Azuma et al. 2003 ; Ong et al. 2005 ;
Pas rather than Mind in the Eyes. In the present data, Muslimovic et al. 2006 ; Williams-Gray et al. 2007), our
by contrast, the Faux Pas deficit fell just short of results reveal that the deficits detected by such tasks
significance once fluid intelligence was controlled. may not be related to their particular cognitive content
Nevertheless, our findings confirm that deficits and that, instead, they might solely reflect a general
on multitasking and theory of mind shown by PD cognitive loss. In our view, neuropsychological as-
patients cannot be fully explained by their loss of fluid sessment in PD should include both fluid intelligence
intelligence. tests and specifics test of multitasking and theory of
Both lesion and neuroimaging studies have pre- mind. Further studies should investigate the contri-
viously linked multitasking and theory of mind to the bution of fluid intelligence to other executive tests
prefrontal cortex. For theory of mind, lesion studies used in PD.
have indicated the particular importance of the orbito- Our data also have powerful implications for the
frontal cortex (e.g. Stone et al. 1998 ; Rowe et al. 2001 ; understanding of the relationship between fluid intel-
Stuss et al. 2001), whereas neuroimaging studies indi- ligence and frontal functions. The previously reported
cate the parallel importance of other regions including results in patients with focal lesions now extend to
the anterior cingulate cortex, the superior temporal PD : whereas some frontal deficits are entirely ex-
sulcus, the temporal poles and the amygdala (Baron- plained by fluid intelligence, others are not. Very
Cohen et al. 1999 ; Gallagher & Frith, 2003 ; Frith & possibly, this dissociation reflects dependence on
Frith, 2006). Multitasking and planning deficits somewhat different frontal regions, with fluid intelli-
have also been described in patients with frontal cor- gence dependent in particular on lateral and dorso-
tex damage (e.g. Hebb & Penfield, 1940 ; Shallice & medial regions (Bishop et al. 2008 ; Woolgar et al. 2010),
Burgess, 1991 ; Goldstein et al. 1993), and the particular whereas more of the anterior frontal cortex is crucial
importance of the anterior prefrontal cortex has been for multitasking and theory of mind. Further studies
suggested by both lesion and neuroimaging studies should investigate such relationships in other clinical
(e.g. Burgess et al. 2007 ; Gilbert et al. 2007 ; Dreher et al. populations with frontal involvement.
2008 ; Badre & D’Esposito, 2009 ; Roca et al. 2011). In
PD, the impairment in these functions has been ex-
plained by the progressive deterioration of fronto- Acknowledgments
striatal circuits that occurs during the course of the
This work was supported by Fundación INECO, and
disease (Bodden et al. 2010 ; Roca et al. 2010b).
the Medical Research Council (MRC) intramural pro-
Although here we have discriminated two groups
gramme MC_US_A060_0001.
of tests, distinguished by whether frontal deficits
are entirely explained by fluid intelligence, a more
realistic possibility may be a continuum. For the
Declaration of Interest
WCST, we found the strongest overlap with fluid in-
telligence, with the patient–control difference far from None.
 Fluid intelligence in Parkinson’s disease 7

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