Defective concept formation in Parkinsonians is independent

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Journal of Neurology, Neurosurgery, and Psychiatry 1989;52:334-337
Defective concept formation in Parkinsonians is
independent from mental deterioration
CARLO CALTAGIRONE, AUGUSTO CARLESIMO, UGO NOCENTINI,
STEFANO VICARI
From the Clinica Neurologica, II Universita di Roma, Rome, Italy
SUMMARY
An extensive neuropsychological battery (the Mental Deterioration Battery) was utilized
to distinguish, within a sample of 24 idiopathic Parkinsonians, those showing signs of diffuse mental
deterioration (n = 9) from those without deterioration (n
=
15). Performances ofcontrol subjects on
a wide range of tests exploring mnesic, visuo-constructive, linguistic and general intellectual functions
(n = 21) did not differ from analogous performances ofParkinsonians without signs of diffuse mental
deterioration. The Wisconsin Card Sorting Test was then used to verify the hypothesis that a selective
impairment of cognitive functions subsumed by the integrity of frontal lobes could be demonstrated
in Parkinsonian patients. Our results provide evidence that in this task, defective performances are
obtained by Parkinsonians and even by patients without signs of diffuse cognitive impairment. These
findings seem to confirm that a deficit in concept formation, maintenance and shifting is largely
independent of the dementia frequently noticed in Parkinson's disease.
It is no longer disputed that there is a prevalence of
dementia in patients affected by Parkinson's disease
which is higher than in the normal population.'
Moreover, even when diffuse mental deterioration has
been absent in Parkinsonian patients, selective deficits
of cognition may be found.2 Some authors claim that
an asymmetrical pattern of cognitive performances
can be found in Parkinsonians with worst scores on
visuo-spatial tasks.34 However, this selective impairmenf of visuo-spatial functions has not been confirmed when the motor-speed component of these tasks
is taken into account.25
Impairment of mnesic functions seems to be better
documented. Long term recall of visual and verbal
material seems to be affected even in the presence of
normal scores on tasks of short term memory and long
term storage.67
After the description by Bowen et ar of a selective
disorder in concept formation in Parkinsonians, many
authors have described these patients as particularly
compromised in tests sensitive to lesions of frontal
Parkinsonians, the weight of a more general mental
deterioration should be checked. In most ofthe studies
pointing to an impairment of frontal functions in
patients affected by Parkinson's disease this factor has
not convincingly been ruled out. The presence of a
more global cognitive impairment has generally been
excluded on the basis of the IQ' derived from the
WAIS, while a detailed survey of mnesic, visuoconstructive and general intellectual functioning is
often missing.8 10
To verify the hypothesis that there is a selective
deficit offunctions normally subsumed by the integrity
of frontal lobes in Parkinsonians, we planned a study
in which a careful evaluation of mental functioning
was performed together with a specific assessment of
concept formation, maintenance and shifting.
Material and methods
Neuropsychological assessment
To assess the presence of a general impairment of mental
functions we used the Mental Deterioration Battery (MDB).
lobes.>"
This consists of eight tasks capable of yielding distinctive
In any case, before positing that a selective impair- information
about mnesic, linguistic, visuo-constructive and
ment of cognitive functions is actually present in general intellectual
functions. The battery has been extenin
described
a
1
sively
Address for reprint requests: Prof C Caltagirone, Institute of MDB tests and the previous study.'2 In table the single
corresponding cognitive functions invesNeurology, II Universita di Roma, Osp S Eugenio, P le dell'Umanetigated are summarised. As demonstrated in a previous
simo 10, 00144 Roma, Italy.
paper,'2 the MDB is able to classify correctly normal and
deteriorated subjects on the basis of the number of pathoReceived 19 January 1988 and in final revised form 8 August 1988.
Accepted 26 August 1988
logical performances. A patient is classified as demented
334
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Defective conceptformation in Parkinsonians is independentfrom mental deterioration
335
Table I Tasks used to build up the MDB: the corresponding Table 3 Mean scores (and standard deviations) normalised
cognitivefunctions investigated by the single tests are indicated in z points obtained on various MDB tasks by control subjects
Word Fluency (WF)
Phrase Construction (PC)
Rey's Verbal/sor
memory test\long
Verbal attainments
Vra tanet
trrealRS)
termn recall (RLT)
Immediate Visual Memory (IVM)
Visuospatial Memory
General Intelligence
on visuospatial data
Copying designsjfree copy (CD)
\copy with landmarks Visuoconstructive
(CDL)
functions
when he obtains four or more pathological performances on
the eight tasks of the MDB. The cutting scores differentiating
normal from pathological performances are derived from
previously published normative data.'2
The test used to assess the ability of concept formation,
maintenance and shifting was the Wisconsin Card Sorting
Test (WCST), which was administered in full measure (128
cards) according to the procedure employed by Milner."3 In
the evaluation of the results we considered the categories
obtained together with the number of perseverative and total
errors produced.
As originally described by Milner,'3 and subsequently
confirmed by other authors"'5 patients with frontal lobe
damage do particularly badly in this test. In these studies the
performance of patients with frontal lobe damage was
indicative of a defective acquirement of categories, and
exhibited a perseverative behaviour in comparison with both
normal subjects and patients with lesions restricted to
posterior regions of the brain.
Subjects
Twenty four consecutive outpatients of the Neurological
Clinic of our University showing clinical evidence of
idiopathic Parkinson's disease were included in our study.
None of them had clinical signs of cerebrovascular disease,
alcoholism or depression nor had they undergone
thalamotomy or other surgical procedures for the relief of
Parkinsonian symptoms.
The mean length of the illness was 4-1 years (SD 1-4). All
the patients demonstrated a level of disability between stages
II and III of the Hoehn and Yahr scale."
Eighteen Parkinsonian patients were in a pharmacological
wash-out period; the others were receiving therapy with
levodopa alone or associated with anticholinergics.
Twenty one subjects, most of them relatives of the
Parkinsonian subjects, without clinical evidence of
Table 2 Age and literacy levels of control and Parkinsonian
subjects
Age (years)
Years of
schooling
Controls
(n = 21)
Parkinsonians
596 (7-8)
7-0 (41)
24)
t
p
615 (7-6)
0.81
6-5 (33)
045
NS
NS
=
Controls
Verbal memory
Coloured Raven's
Progressive Matrices (PM'47)
(n
and Parkinsonian patients; statistical comparisons on
Student's t test are also reported
(n
WF
CF
RST
RLT
IVM
PM'47
CD
CDL
=
21)
016 (10)
0-15 (1-0)
0 31 (1-0)
0-17(0.97)
015(086)
0-25 (0 79)
0-23 (0-58)
0-23 (0 84)
Parkinsonians
(n = 24)
t
p
-0-14 (0-95)
-0 13 (0-97)
-0-27 (0 89)
10
0 99
2-05
108
1-04
0-96
1-62
1-49
NS
NS
-014(10)
-0-19 (1-0)
-0-13(1-1)
-0.21 (1-1)
-0-20 (1-2)
<0-05
NS
NS
NS
NS
NS
neurologic or psychiatric disorders were used as the control
group.
Results
Although the age and literacy levels demonstrated by
Parkinsonians and control subjects were comparable
(table 2), performance scores for the two groups on the
various tasks of the MDB were adjusted for age and
years of schooling on the basis of the standard
procedures reported in a previous paper.'2 Moreover,
so that results obtained in tests having different ranges
could be compared, the adjusted scores were transformed into normalised Z scores.
The results obtained on various MDB tests by both
Parkinsonian and control groups are summarised in
table 3.
Parkinsonian patients obtained lower scores than
control subjects on most of the tasks. A two-way
analysis of variance, in which the results obtained in
the eight MDB tests were taken into consideration,
reveals that the difference between the two groups
approaches the level of significance (F = 3-6; p =
006). These results are in agreement with the data of
several other authors."7'8
Brown and Marsden2 suggested that in non-selected
Table 4 Mean scores (and standard deviations) normalised
in z points obtained on various MDB tasks by control subjects
and non-demented Parkinsonian patients; statistical
comparisons on Student's t test are also reported
Controls
(n= 21)
WF
CF
RST
RLT
IVM
PM'47
CD
CDL
0-16 (1-0)
0-15(1.0)
0.31 (1-0)
0-17 (0-97)
0-23 (0 84)
0.15 (0-86)
0 25 (0-79)
0-23 (0-58)
Non-demented
Parkinsonians
(n= 15)
t
p
0-10 (0-91)
0.36(0-74)
0-18 (0-75)
0-29 (0.83)
0 33 (0-69)
0 40 (0-95)
0-27 (0-80)
0-35 (0-82)
0-20
0-64
0-41
NS
NS
NS
NS
NS
NS
NS
NS
0-39
0 40
0-80
0-05
0-61
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Caltagirone, Carlesimo, Nocentini, Vicari
number of pathological performances below four and
then were classified as non deteriorated.
A comparison of performances on the various MDB
0tasks obtained by control subjects and non-Controls
o-----0-2deteriorated Parkinsonians is reported in table 4. A
Parkinsonians
*
*o
ND
two-way analysis of variance does not reveal any
-0.4D
Parkinsonians
significant difference for any factor (F always < 1).
-0-6No significant difference can be detected even in the
-0.8comparisons of single tests.
Profiles exhibited on the various tasks of MDB by
-1.
control subjects and Parkinsonian patients are shown
WF PC RST RLT IVM PM CD CDL in the figure. Profiles of performances obtained by
controls and non deteriorated Parkinsonians are
Fig Neuropsychological profiles exhibited on the MDB by
almost superimposable while the profile shown by
our samples ofcontrol subjects and Parkinsonian patients
affected (D) or not (ND) by mental deterioration.
deteriorated Parkinsonians is quite different from
these.
The WCST results for the three groups, control
populations mean performance values may be affected subjects,
non-demented and demented Parkinsonians,
significantly by the inclusion of subjects suffering from are summarised
in table 5.
mental deterioration. Since the purpose of our study
scores obtained did not fit a
that
Given
performance
in
was to detect a possible selective deficit in cognition
was performed
statistical
distribution,
normal
Parkinsonian patients without clinical and neuro- by means of a non parametric analysis
test (Mann-Whitney U
psychological signs of dementia, we subdivided the test).
total sample of Parkinsonians into two groups. On the
Non-deteriorated Parkinsonians produced sigbasis of MDB performance, the patients of the total nificantly
more perseverative errors and obtained
sample were identified as being affected or not by fewer categories
(this difference only approaches statof
was
composed
The
first
group
deterioration.
mental
significance:
p = 0-07) than control subjects. In
istical
15 patients classified as not deteriorated while the the comparison between
performance scores demonremaining nine patients, classified as deteriorated, strated by the two subgroups
the
made up the second group. The prevalence of de- difference regarding the numberofofParkinsonians
categories and of
mentia in our group of Parkinsonians is comparable perseverative errors approaches
significance
with that reported in larger samples.'920
(categories: p = 005; perseverative errors: p = 0.06),
The two subgroups of Parkinsonians did not differ while
the difference in the number of total errors
as regards mean age (non deteriorated: 60-0, SD 8 1;
reaches the level of statistical significance. No sigdeteriorated: 63 5, SD 6-9; t = 1 -1, p = NS) and years nificant
difference was detected in the number of total
of schooling (non deteriorated: 6-9, SD 2-2;
between normal subjects and non-deteriorated
deteriorated: 5-7, SD 2-0; t = 1-4, p = NS). Non errors
deteriorated Parkinsonians had a mean duration of Parkinsonians.
disease (3-6 years; SD 1.2) significantly shorter than
deteriorated ones (4-8 years; SD 1 3) (t = 2 3; p = Discussion
0-03). Thirteen of the non deteriorated Parkinsonians
were in a pharmacological wash-out period while the
Several authors have described impaired performremaining two patients were receiving levodopa.
ances on "frontal tasks" in patients affected by
In the deteriorated group, five patients were in a Parkinson's disease which did not show clinical and
pharmacological wash-out period. The remaining four neuropsychological signs of general intellectual
patients were receiving levodopa alone (two patients) deterioration. Bowen et a15 found that Parkinsonian
or in association with anticholinergics (two patients).
patients formed significantly fewer concepts, as
All the control subjects demonstrated on the MDB a measured by WCST, than controls matched for age,
336
0.40.2-
--
-1 *0
Table 5 Medians (and ranges) ofscores obtained on WCST by control subjects, non-deteriorated and deteriorated
Parkinsonians; statistical comparisons on Mann- Whitney U test are also indicated
Control
subjects
(n = 21)
Categories
Total errors
Perseverative errors
5-8 (3-6)
360 (1-72)
10-0(0-52)
z
p
Non-demented
Parkinsonians
(n = 15)
1-8
1-4
2-0
NS
NS
=004
50 (1-6)
420 (14-82)
250 (3-71)
z
p
Demented
Parkinsonians
(n = 9)
1.9
2-0
1-8
NS
= 004
NS
20(0-5)
580 (38-74)
340 (22-40)
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Defective conceptformation in Parkinsonians is independentfrom mental deterioration
337
literacy and verbal WAIS IQ. For Parkinsonian patients. " Furthermore, a reduction of dopamine
patients with normal IQ Lees and Smith9 reported content and of its metabolites in frontal cortical areas
difficulty in shifting conceptual sets and a per- has been found in the brain ofParkinsonian subjects.2'
severative behaviour on both the modified WCST and This finding is probably related to the degeneration of
Benton's Word Fluency test. A similar shifting a mesocortical dopaminergic pathway projecting from
aptitude disorder was observed in tests of block and the mesencephalon to cingulate, entorhinal and frontal cortex.22
animal sorting and finger pushing sequences.'"
In these studies a general intellectual impairment
was excluded on the basis of a normal WAIS IQ.
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Defective concept formation in
parkinsonians is independent
from mental deterioration.
C Caltagirone, A Carlesimo, U Nocentini and S Vicari
J Neurol Neurosurg Psychiatry 1989 52: 334-337
doi: 10.1136/jnnp.52.3.334
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