Neuropsychologia 47 (2009) 406–414
Contents lists available at ScienceDirect
Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia
Are dopaminergic pathways involved in theory of mind? A study in Parkinson’s
disease夽
Julie Péron a,b , Siobhan Vicente a,b,c , Emmanuelle Leray b,d , Sophie Drapier a,b , Dominique Drapier b,d ,
Renaud Cohen e, Isabelle Biseul b, Tiphaine Rouaud a,b, Florence Le Jeune b,f, Paul Sauleau a,b, Marc Vérin a,b,∗
a
Clinique Neurologique, Hôpital Pontchaillou, CHU de Rennes, Rue Henri Le Guilloux, 35033 Rennes, France
Unité de Recherche Universitaire 425 “Comportement et Noyaux Gris Centraux”, Université Rennes 1, Hôpital Pontchaillou, CHU de Rennes,
Rue Henri Le Guilloux, 35033 Rennes, France
c
S.H.U. Psychiatrie Adulte, CH Guillaume Régnier, 108 Avenue du Général Leclerc, 35703 Rennes, France
d
Service d’Epidémiologie et de Santé Publique, Hôpital Pontchaillou, CHU de Rennes, Rue Henri Le Guilloux, 35033 Rennes, France
e
Département de Psychologie, Ile du Saulcy, Université Paul Verlaine, 57045 Metz Cedex 1, France
f
Service de Médecine Nucléaire, Centre Eugène Marquis, Rue de la Bataille Flandres Dunkerque, 35042 Rennes, France
b
a r t i c l e
i n f o
Article history:
Received 24 March 2008
Received in revised form 15 July 2008
Accepted 12 September 2008
Available online 18 September 2008
Keywords:
Emotion
Dopamine
Theory of mind
a b s t r a c t
The “orbitofrontal” and “cingulate” frontostriatal loops and the mesolimbic dopaminergic system that
modulates their function have been implicated in theory of mind (ToM). Parkinson’s disease (PD) provides
a model for assessing their role in humans. Results of the handful of previous studies of ToM in PD providing
preliminary evidence of impairment remain controversial, mainly because the patients included in these
studies were not accurately described, making it difficult to determine whether their ToM deficits were
due to general cognitive deterioration or to a more specific dopaminergic deficit. The aim of our study was
therefore to re-examine previous results highlighting ToM in PD and to explore the involvement of the
dopaminergic pathways in ToM. ToM was investigated in 17 newly diagnosed PD patients (early PD group),
27 PD patients in the advanced stages of the disease (advanced PD group) and 26 healthy matched controls
(HC), using two ToM tasks: a visual one, which is thought to reflect the “affective” ToM subcomponent
(“Reading the Mind in the Eyes”), and a verbal one, which is thought to reflect both the “affective” and the
“cognitive” ToM subcomponents (faux pas recognition). Furthermore, the early PD group was studied in
two conditions: with and without dopamine replacement therapy (DRT). We failed to find any significant
difference in ToM between the early PD patients and the HC group. Furthermore, there was no difference
between the early PD patients in the medicated and unmedicated conditions. Conversely, the advanced
PD patients scored poorly on the intention attribution question (“cognitive” ToM score) in the faux pas
recognition task. The present results suggest that the deficit in ToM only occurs in the more advanced
stages of the disease. In addition, our results would appear to indicate that these advanced PD patients
present “cognitive” ToM impairment rather than global (“cognitive” and “affective”) ToM impairment. In
other words, the ToM deficit would appear to be present in PD patients where the degenerative process has
spread beyond the dopaminergic pathways, but not in early PD patients where neuronal loss is thought to
be restricted to the nigrostriatal and mesolimbic dopaminergic systems. In conclusion, our results suggest
that the dopaminergic pathways are not involved in ToM.
© 2008 Elsevier Ltd. All rights reserved.
1. Introduction
Abbreviations: PD, Parkinson’s disease; ToM, theory of mind; HC, healthy controls; DRT, dopamine replacement therapy.
夽 This study was carried out at the Clinique Neurologique, Hôpital Pontchaillou,
CHU de Rennes, Rue Henri Le Guilloux, 35033 Rennes, France.
∗ Corresponding author at: Clinique Neurologique, Hôpital Pontchaillou, CHU de
Rennes, Rue Henri Le Guilloux, 35033 Rennes, France. Tel.: +33 2 99 28 42 93
fax: +33 2 99 28 41 32.
E-mail address: [email protected] (M. Vérin).
0028-3932/$ – see front matter © 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuropsychologia.2008.09.008
The term “theory of mind” (ToM) refers to the cognitive ability to represent one’s own and other people’s mental states – for
instance, in terms of thinking, believing or pretending. Interestingly, the term was first used by a primatologist and a psychologist:
Premack and Woodruff (1978). ToM is also referred to as “mentalizing” (Frith, Morton, & Leslie, 1991), “mind-reading” (Frith &
Happe, 1994; Singer, 2006; Vogeley et al., 2001), “social intelligence” (Baron-Cohen, O’Riordan, Stone, Jones, & Plaisted, 1999),
J. Péron et al. / Neuropsychologia 47 (2009) 406–414
and “Machiavellian intelligence” (Brune, 2001). ToM is thought
to have distinct functional subcomponents (Brothers & Ring,
1992; Coricelli, 2005). Depending on task demands, ToM may
require emotional (“affective ToM”) or cognitive (“cognitive ToM”)
perspective-taking, or both. Cognitive aspects of ToM are referred
to as “cold”, and correspond to knowledge about others’ beliefs
or intentions, whereas affective aspects of ToM are referred to as
“hot”, and correspond to the appreciation of the others’ emotional
states.
A number of neuroimaging studies have examined the neural systems engaged during the representation of other people’s
mental states, compared with situations requiring no such representation (Brunet, Sarfati, Hardy-Bayle, & Decety, 2000; Calarge,
Andreasen, & O’Leary, 2003; Fletcher et al., 1995; Gallagher
& Frith, 2003; Goel, Grafman, Sadato, & Hallett, 1995; Harris,
Todorov, & Fiske, 2005; Hynes, Baird, & Grafton, 2006; Vollm et
al., 2006). Similarly, impaired ToM has been described in adult
patients with focal lesions in the frontal lobe (Bird, Castelli,
Malik, Frith, & Husain, 2004; Farrant et al., 2005; Happe, Malhi,
& Checkley, 2001; Mazza et al., 2006; Rowe, Bullock, Polkey, &
Morris, 2001; Shamay-Tsoory & Aharon-Peretz, 2007; ShamayTsoory, Tomer, Berger, & Aharon-Peretz, 2003; Stuss, Gallup, &
Alexander, 2001) and in the amygdala (Fine, Lumsden, & Blair, 2001;
Shaw et al., 2004; Stone, Baron-Cohen, Calder, Keane, & Young,
2003), as well as in patients with neurodegenerative pathologies
known to involve the orbitofrontal and cingulate frontostriatal
loops, together with the mesolimbic dopaminergic system which
modulates the activity of these loops: the frontal variant of frontotemporal dementia (Eslinger et al., 2006; Lough, Gregory, &
Hodges, 2001; Lough et al., 2006; Snowden et al., 2003; Torralva
et al., 2006), Huntington’s disease (Snowden et al., 2003) and
Parkinson’s disease (PD) (Mengelberg & Siegert, 2003; Mimura,
Oeda, & Kawamura, 2006; Saltzman, Strauss, Hunter, & Archibald,
2000).
These studies have highlighted the role played by the superior
temporal sulcus and temporal poles, the amygdala, the prefrontal
cortex (especially the paracingulate cortex) and the “orbitofrontal”
and “cingulate” loops (Cummings, 1993) in the representation of
other people’s mental states. Neuroimaging (Hynes et al., 2006;
Vollm et al., 2006) and lesion studies (Shamay-Tsoory & AharonPeretz, 2007; Shamay-Tsoory, Tomer, Berger, Goldsher, & AharonPeretz, 2005) have also provided evidence for the existence of a
dissociation between the cognitive and affective aspects of ToM.
Using fRMI, Hynes et al. (2006) demonstrated that the orbitofrontal
cortex is involved in affective, rather than cognitive, perspectivetaking. Lastly, it has also been suggested that the mesolimbic and
nigrostriatal dopaminergic systems, which modulate the activity
of the two loops, may be involved in ToM (Owen, 2004; Pezze &
Feldon, 2004).
As PD is a neurodegenerative affection involving both the nigrostriatal and mesocorticolimbic dopaminergic systems, it offers an
opportunity to study the possible influence of dopaminergic pathways on cognitive functions such as ToM. Three previous studies of
PD patients seem to have yielded preliminary evidence of impaired
ToM. However, the patients included in these studies were not
accurately described and the PD group was not homogeneous in
terms of age, severity of the disease, duration of the disease and
dopa sensitivity. In addition, the PD patients included in these studies displayed major dysexecutive syndromes and mood disorders,
making it difficult to determine whether the ToM deficits were due
to a specific dopaminergic deficit or to an overall cognitive deterioration in the advanced stages of the disease, owing to the extension
of the lesions to non-dopaminergic pathways (Braak et al., 2003).
In this context, several questions remained unanswered: do the
ToM deficits observed in PD stem from the progression of the dis-
407
ease and the cortical extension of the lesions rather than from
specific dopaminergic depletion? If ToM deficits can indeed be
observed in PD, which subcomponents of ToM are impaired: the
affective one, the cognitive one or both?
The aim of our study was to explore the involvement of the
dopaminergic pathways in ToM by studying PD patients at different stages of the disease: newly diagnosed patients (early PD) and
patients with advanced pathology (advanced PD), but also early PD
patients with and without dopamine replacement therapy (DRT),
compared with healthy controls (HC).
We sought to re-examine previous results highlighting ToM in
PD by using two ToM tasks. The first task (Reading the Mind in
the Eyes (Baron-Cohen et al., 2001)) was intended to reflect the
“affective” subcomponent of ToM, while a second task (faux pas
recognition task (Baron-Cohen, Jolliffe, Mortimore, & Robertson,
1997)) was intended to reflect both the “cognitive” and “affective”
subcomponents of ToM.
2. Methods
2.1. Participants
Two groups of PD patients at different stages of the disease (early and advanced
PD groups) and a healthy control (HC) group took part in the study.
The characteristics of the two patient groups and the HC group are presented in
Table 1.
2.1.1. PD patients (Table 1)
Inclusion criteria for PD patients were idiopathic PD (Hughes et al., 1992), preserved dopa reactivity, lack of dementia (score > 130 on the Mattis Dementia Rating
Scale) (Mattis, 1988) and, for the early PD group only, the ability to be tested not
only in the “on” dopa condition (maximum therapeutic effect of dopaminergic treatment) but also in the “off” dopa condition (after approximately 12 h of therapeutic
withdrawal).
The early PD group consisted of 17 non-demented patients with PD. Severity
of the disease was rated using both the revised Hoehn & Yahr disability scale (H&Y,
Hoehn & Yahr, 1967) and the Schwab & England scale (S&E, Schwab & England, 1969).
The early PD group was examined in two conditions: a medicated condition and an
unmedicated one. Note that the terms “medicated” and “unmedicated” only refer
to daily DRT for PD (levodopa preparations and/or dopamine receptor agonists). In
the medicated condition, all patients were receiving anti-Parkinsonian medication
and all were stable on their medication and good responders. Medication intake
was defined as the DRT, calculated on the basis of correspondences adapted from
Lozano et al. (1995). For the unmedicated condition, patients were asked to abstain
from taking their medication the night before the assessment was scheduled to take
place. Levodopa is eliminated from plasma with a half-life of 1–2 h (Gancher, Nutt,
& Woodward, 1987).
The advanced PD group consisted of 27 non-demented patients with PD. Severity
of the disease was also rated using both the revised Hoehn & Yahr disability scale
(H&Y, Hoehn & Yahr, 1967) and the Schwab & England scale (S&E, Schwab & England,
1969). All patients were receiving anti-Parkinsonian medication, which was defined
in the same way as for the early PD group (DRT).
2.1.2. HC participants (Table 1)
The HC group consisted of 26 healthy individuals who had no history of neurological disease, head injury or alcohol abuse, and no signs of dementia as attested
by their scores on the MMSE (Dérouesné, 2001).
All groups were comparable for age and education level. After they had been
given a full description of the study, written informed consent was obtained from
each participant, and the study was conducted in accordance with the Declaration
of Helsinki.
2.2. Theory of mind (ToM) tasks
Two ToM tasks were used in the experiment. The first task (i.e. the faux pas
recognition task (Baron-Cohen et al., 1997)) is thought to reflect both the “cognitive”
and “affective” subcomponents of ToM, The second task (i.e. the Reading the Mind
in the Eyes test (Baron-Cohen, Wheelwright, Hill, Raste, & Plumb, 2001)) is thought
to reflect solely the “affective” subcomponent of ToM.
2.2.1. Faux pas recognition test (“Cognitive” and “affective” verbal ToM task)
In this test, participants are read a story which may or may not contain a social
faux pas (Baron-Cohen et al., 1999; Farrant et al., 2005; Stone et al., 2003; Stone,
Baron-Cohen, & Knight, 1998). A faux pas story could feature someone being rude
about a wedding gift, forgetting that they are speaking to the person who gave
408
J. Péron et al. / Neuropsychologia 47 (2009) 406–414
Table 1
Clinical and demographic data (mean ± S.D.) for the two patient groups and the control group. Differential effects between the three groups are reported (Kruskal–Wallis and
Mann–Whitney U test).
Early PD (n = 17)
Advanced PD (n = 27)
HC (n = 26)
Stat. Value
Mean
S.D.
Range
Mean
S.D.
Range
Mean
S.D.
Range
Sex (F/M)
Age (years)
Education (years)
Handedness (R/L)
Disease duration (years post-onset)
DRT (mg)
5M/12F
61.0
11.5
17 R
2.5
458a
–
7.1
4.0
–
1.5
337a
–
37–67
9–20
–
0.1–5
120–1300
18M/9F
56.6
11.0
27 R
10.2
1104
–
7.8
4.5
–
4.9
509
–
44–69
6–20
–
3–18
50–1860
13M/13F
59.8
12.2
26 R
–
–
–
6.8
2.9
–
–
–
–
41–70
9–16
–
–
–
H&Y rating score
On
Off
1.0
1.5
0.9
0.7
0–2.5
0–2.5
1.3
2.5
0–4
1–5
–
–
–
–
S&E rating score (%)
On
Off
MADRS
92.4
85.9
4.9
5.6
8.0
3.1
80–100
70–100
0–10
87.8
58.1
4.6
60–100
10–90
0–10
–
–
–
–
–
–
0.9
1.0
11.5
25.3
3.9
–
4.5
2.1
p-Value
–
.10
.34
29.2
13.6
.000*
.000*
–
–
206.0
108.0
.55
.003*
–
–
–
184.0
63.5
101.5
.24
.000*
.71
Abbreviations: PD: Parkinson’s disease; HC: healthy controls; DRT: dopamine replacement therapy; H&Y: Hoehn and Yahr; S&E: Schwab and England. MADRS:
Montgomery–Asberg Depression Rating Scale; S.D.: standard deviation.
a
For the medicated condition.
*
Significant if p value less than 0.05.
it to them (see example below). The story is placed in front of participants so
that it may be referred to if necessary, thereby reducing the demands made on
working memory (Stone et al., 2003). We used a shortened version of the test,
comprising 5 stories with a faux pas and 5 control scenarios without a faux pas.
A second equivalent version of this test was used to assess the early PD patients in
the unmedicated condition. After each story, participants were asked the following
questions:
1. “Did anyone say something s/he should not have said or something awkward?”
(faux pas detection test). If the participants answered “yes”, they were asked the
following questions:
2. “Who said something s/he should not have said or something awkward?” (faux
pas comprehension test).
3. “Why shouldn’t s/he have said it or why was it awkward?” (faux pas comprehension test).
4. “Why do you think s/he said it?” (faux pas comprehension test).
5. “Did X know that Y. . .?” (test for realising that the faux pas was unintentional).
6. “How did X feel?” (test for attributing emotions to the protagonists).
Questions 7 and 8 were control questions to check that participants understood the details of the story. Participants were asked a question about some
important detail of the story, such as “What had Jeanette given Anne for her
wedding?”
Example: Jeanette bought her friend Anne a crystal bowl for a wedding gift.
Anne had a big wedding and there were a lot of presents to keep track of. About a
year later, Jeanette was over one night at Anne’s for dinner. Jeanette dropped a wine
bottle by accident on the crystal bowl, and the bowl shattered. “I’m really sorry, I’ve
broken the bowl,” Jeannette said. “Don’t worry,” said Anne, “I never liked it anyway.
Someone gave it to me for my wedding.”
Questions 2–6 were only asked if participants detected the faux pas, i.e. if they
answered “Yes” to Question 1. If not, the experimenter skipped to Questions 7 and
8 (the control questions).
In order to realise that a faux pas has occurred, participants have to represent
two mental states. First that the person making the remark does not realise that
s/he should not have made it “cognitive” ToM; intentionality score. Second, that
the person hearing it is bound to feel hurt or insulted (“affective” ToM; emotion
attribution score) (Shamay-Tsoory & Aharon-Peretz, 2007).
Scoring: we adopted the scoring system used by Stone et al. (1998), whereby
performances on each component of the test are calculated separately as follows
(Stone et al., 1998):
1. Correct hits score: for each story with a faux pas, one point was given for each
correct answer. The maximum “correct hits” score on the test was therefore 30
(6 questions × 5 faux pas stories, maximum = 30), and scores were converted into
a percentage of correct responses.
2. Correct rejects score: for each neutral story, two points were given for each correct
answer. The maximum “correct rejects” score on the test was therefore 10 (1
question × 5 neutral stories, maximum = 10), and scores were converted into a
percentage of correct responses.
3. Correct faux pas story control score: for each story with a faux pas, one point was
given for each correct answer to the two control questions. The maximum “correct
faux pas story control” score on the test was therefore 10 (2 control questions × 5
faux pas stories, maximum = 10), and scores were converted into a percentage of
correct responses.
4. Correct neutral story control score: for each neutral story, one point was given for
each correct answer to the two control questions. The maximum “correct neutral
story control” score on the test was therefore 10 (2 control questions × 5 neutral
stories, maximum = 10), and scores were converted into a percentage of correct
responses.
Several composite scores and subscores were also calculated.
The correct hits score was broken down into four subscores as follows:
(1a)
(1b)
(1c)
(1d)
Detection score (question 1 × 5 faux pas stories, maximum = 5),
Explanation score (questions 2 to 6 × 5 faux pas stories, maximum = 25),
Intention attribution score (question 5 × 5 faux pas stories, maximum = 5),
Emotion attribution score (question 6 × 5 faux pas stories, maximum = 5).
A composite “total detection” score was calculated as follows: the detection
score plus the correct rejects score (maximum = 15). Lastly, a composite “total control
questions” score was calculated as follows: the correct faux pas story control score
plus the correct neutral story control score (maximum = 20).
All these additional scores were converted into a percentage of correct
responses.
Control tasks: To check that the early processing stages of verbal abilities were
intact (abilities required for the faux pas recognition task), the abridged version
of the Token Test (De Renzi & Vignolo, 1962) and the verbal modality of the Pyramids and Palm Trees Test (PPTT, Howard & Patterson, 1992) were administered to all
participants. The former assesses syntax comprehension and requires participants
to point to tokens corresponding to a verbal instruction (e.g. “Touch the large red
square”), while the latter measures semantic access from words and requires participants to match one item (word) with one of two others (e.g. a pyramid with a palm
tree or a pine tree). None of the patients included in the study presented any deficit
in syntax comprehension, as measured by the Token Test, or in semantic access, as
measured by the verbal PPTT.
2.2.2. Reading the Mind in the Eyes test (“affective” visual ToM task)
A French adaptation of the revised version of the Reading the Mind in the Eyes
test was used (Baron-Cohen et al., 2001; Cohen et al., 2006). We used a shortened,
computerised version, comprising 17 photographs of the eye region of the faces of
actors and actresses. A second equivalent version of this test was used to assess
the early PD patients in the unmedicated condition. The stimuli were depicted on
separate slides and presented one after the other. Four adjectives corresponding to
complex mental state descriptors (e.g. hateful, panicked) were printed on each slide,
with one adjective in each corner and the photo in the middle. One of these words
(the target word) correctly described the mental state of the person in the photograph, while the others were included as foils. It was possible for the three foils to
have the same emotional valence as the target word. Participants were required to
decide which of the four words best described what the individual in the photograph
was thinking or feeling, and there was no time limit. Participants were instructed
to read the chosen word aloud. This task is regarded as an advanced ToM task, as
participants have to try and put themselves in the shoes of the person shown in the
photograph and attribute a relevant complex mental state to him/her. As a control
J. Péron et al. / Neuropsychologia 47 (2009) 406–414
task, participants judged the gender of the person shown in the photograph (gender attribution task). Before the test, participants read through a glossary which
contained the meanings of the words describing the mental states. If necessary,
the glossary could be used during the assessment (for a detailed description, see
Baron-Cohen et al., 2001).
Scoring: The test was scored by totalling the number of items (photographs)
that had been correctly identified by the participant, i.e. the number of correctly identified mental states. The maximum “emotion score” on the test was
therefore 17, which was converted into a percentage of correct responses. In
addition, a control score was calculated by totalling the number of correct
responses in the gender attribution task. The maximum “gender score” on the test
was therefore 17, and scores were again converted into a percentage of correct
responses.
Control task: To check that the early processing stages of face perception were
intact, and to supplement the gender attribution task included in the Reading the
Mind in the Eyes test, the Benton Facial Recognition Test (Benton, Hamsher, Varney,
& Spreen, 1983) was administered to all participants. This task requires participants
to match pictures of the same individuals’ faces, taken from different angles and
in different lighting conditions. None of the patients included in the study presented any aperceptive prosopagnosia, as measured by the Benton Recognition
Test.
2.3. Neuropsychological background and psychiatric assessment
Prior to the ToM assessment, a short neuropsychological and psychiatric battery was administered to the two patient groups (i.e. the advanced PD group
and the early PD group in the medicated condition). Performances by the
participants on the neuropsychological and psychiatric tests are presented in
Table 2.
The battery included the Mattis Dementia Rating Scale (Mattis, 1988) and a
series of tests assessing executive functions: the Modified Wisconsin Card Sorting Test (Nelson, 1976), the Trail Making Test (Reitan, 1958), categorical and literal
fluency tasks (Cardebat, Doyon, Puel, Goulet, & Joanette, 1990), the action (verb) fluency task (Woods et al., 2005) and the Stroop Test (Stroop, 1935). In the unmedicated
condition, only the Mattis Dementia Rating Scale (Mattis, 1988) was administered
to the early PD patients. Depression was assessed using the Montgomery–Asberg
Depression Rating Scale (MADRS, Montgomery & Asberg, 1979). The MADRS was
409
chosen because of the predominance of psychic over somatic items, thus limiting
interference with Parkinson’s symptoms.
2.4. Procedure
In order to avoid a list effect between the “on” dopa and “off” dopa conditions in
the early PD patient group, these were counterbalanced in each of the ToM tasks. In
the “on” dopa condition, half the early PD patients were assessed with Version “A”
of the ToM tasks and half with Version “B”. In the “off” condition, the former were
assessed with Version “B” and latter with Version “A”. The same counterbalancing
method was applied to the advanced PD group and the HC group: the advanced PD
patient group and the HC group were both divided into two groups, half of each
group were assessed with Version “A” and half with Version “B”.
The protocol was completed in a single 90-min session. The early PD patients in
the unmedicated condition underwent a second 60-min session.
2.5. Statistical analysis
Given the small size of the three samples (<30), normality could not be assumed
and we therefore performed non-parametric statistical analyses.
The scores for the neuropsychological background and the sociodemographic
data (except for age and education level) were compared using the non-parametric
Mann–Whitney U test for two independent groups, i.e. the early PD group and the
advanced PD group.
The scores for the remaining sociodemographic data (age and education level),
the control tasks and the ToM tasks were first compared using the Kruskal–Wallis
non-parametric one-way analysis by ranks for the three independent groups, i.e.
the early PD group in the medicated condition, the advanced PD group and the HC
group. If there was a significant group effect, paired comparisons were performed
using the non-parametric Mann–Whitney U test for two independent groups. The
same analyses were carried out with the early PD group in the unmedicated
condition.
For the intragroup comparisons, Wilcoxon’s test for paired samples was used to
assess the effect of the experimental condition (medicated vs. unmedicated) in the
early PD group.
Correlations between (1) control tasks and ToM, and (2) neuropsychological
background and ToM were assessed using Spearman’s rank correlation coefficient.
Table 2
Neuropsychological data (mean ± S.D.) for the two patient groups and the control group. Differential effects between the three groups are reported (Kruskal–Wallis and
Mann–Whitney U test).
Early PD (n = 17)
Statistical
Valuea
p-Valuea
Statistical
Valueb
p-Valueb
0.8
4.4
1.0
0.5
–
–
0.4
0.7
2.4
229.0
–
.8
.7
.3
1.0
–
1.2
0.2
0.0
1.2
–
.6
.9
1.0
.2
Advanced PD (n = 27)
HC (n = 26)
Mean
S.D.
Mean
S.D.
Medicated
Unmedicated
Mean
S.D.
Mean
S.D.
M.M.S.E
Benton
Token Test
PPTT verbal
Mattis
–
45.4
34.6
51.1
138.8
–
4.4
1.8
1.4
4.4
–
47.2
35.1
51.5
140
–
4.4
1.0
1.0
4.5
–
45.8
35
51.7
139.1
–
3.1
1.3
0.4
4.1
28.9
46.4
35.0
51.7
–
Stroop Test
Word
Colour
ColourWord
Interference
110.9
76.3
39.7
−6.1
14.0
12.0
13.1
12.4
–
–
–
–
–
–
–
–
104.5
72.0
44.6
2.4
14.7
13.0
13.0
10.1
–
–
–
–
–
–
–
–
174.0
187.0
190.5
130.5
.2
.3
.3
.02*
–
–
–
–
–
–
–
–
TMT (s)
A
B
B–A
50.4
108.7
58.2
19.4
38.0
28.7
–
–
–
–
–
–
45.4
103.8
58.4
14.8
38.0
31.4
–
–
–
–
–
–
191.5
208.0
227.0
.4
.6
.9
–
–
–
–
–
–
26.8
19.9
14.1
7.8
6.6
4.1
–
–
–
–
–
–
26.3
20.4
11.0
11.6
8.3
5.2
–
–
–
–
–
–
206.0
222.0
131.5
.6
.9
.02*
–
–
–
–
–
–
5.5
6.0
2.3
1.1
7.7
4.6
–
–
–
–
–
–
5.6
5.5
1.6
1.1
6.0
2.0
–
–
–
–
–
–
216.5
228.5
225.5
–
–
–
–
–
–
Verbal fluency
Categorical
Phonemic
Action verb fluency
W.C.S.T
Number of categories
Number of errors
Number of perseverations
.7
1.0
.9
Abbreviations: PD: Parkinson’s disease; HC: healthy controls; M.M.S.E: Mini Mental State Examination; PPTT: Pyramids and Palm Trees Test; TMT: Trail Making Test; W.C.S.T:
Modified Wisconsin Card Sorting Test; S.D.: standard deviation.
a
Comparisons (Kruskal–Wallis non-parametric one-way analysis) were performed between the three independent groups, i.e. the early PD group in the medicated
condition, the advanced PD group and the HC group.
b
Comparisons (Kruskal–Wallis non-parametric one-way analysis) were performed between the three independent groups, i.e. the early PD group in the unmedicated
condition, the advanced PD group and the HC group.
*
Significant (p < 0.05).
410
J. Péron et al. / Neuropsychologia 47 (2009) 406–414
Table 3
Performances of the two patient groups and the control group on ToM tasks (i.e. faux pas recognition test and “Reading the Mind in the Eyes” test). Differential effects between
the three groups are reported (Kruskal–Wallis and Mann–Whitney U test).
Early PD (n = 17)
Medicated
Unmedicated
Advanced PD (n = 27)
HC (n = 26)
Mean (%)
S.D.
Mean (%)
S.D.
Statistical
valuea
p-Valuea
Statistical
valueb
p-Valueb
Mean (%)
S.D.
Mean (%)
S.D.
Faux pas test
Correct hits
Correct rejects
Faux pas story control questions
Neutral story control questions
Faux pas story detection
Explanation
Intention attribution (ToM)
Emotion attribution (affective ToM)
Total detection score
Total control questions
82.7
96.5
96.5
98.8
88.2
84.3
74.1
81.1
93.7
97.6
16.7
10.6
8.6
3.3
15.9
16.8
22.1
18.0
7.6
5.0
91.3
96.9
98.5
98.5
95.4
92.8
83.1
90.8
96.4
98.5
8.8
7.5
3.8
5.5
8.8
9.6
11.1
17.5
5.2
3.2
77.3
94.8
97.0
98.1
85.9
79.3
64.4
75.6
91.9
97.6
22.8
8.9
7.2
5.6
19.9
23.7
27.9
27.9
8.1
4.2
88.8
90.8
97.7
98.1
91.5
90.8
81.5
87.7
91.0
97.9
10.6
14.1
6.5
6.5
10.1
10.2
17.8
15.0
10.3
4.0
4.20
2.80
0.45
0.01
0.57
3.18
5.58
2.56
0.65
0.20
.1
.2
.8
1.0
.8
.2
.06
.3
.7
.9
5.40
2.11
0.39
0.12
2.83
4.77
7.25
4.41
3.08
0.32
.07
.4
.8
.9
.2
.09
.03*
.1
.2
.9
Eyes test
Gender score
Emotion score
96.2
64.0
3.6
15.7
93.7
69.7
11.6
15.0
95.4
66.9
5.0
14.2
96.2
65.2
5.2
12.3
0.55
0.24
.8
.8
0.80
1.20
.7
.5
Abbreviations: PD: Parkinson’s disease; HC: healthy controls; ToM: theory of mind; S.D.: standard deviation.
a
Comparisons (Kruskal–Wallis non-parametric one-way analysis) were performed between the three independent groups, i.e. the early PD group in the medicated
condition, the advanced PD group and the HC group.
b
Comparisons (Kruskal–Wallis non-parametric one-way analysis) were performed between the three independent groups, i.e. the early PD group in the unmedicated
condition, the advanced PD group and the HC group.
*
Significant (p < 0.05).
In order to compare the two parallel versions (A & B) of each of the ToM tasks,
paired comparisons within the HC group (n = 26) were performed using the nonparametric Mann–Whitney U test for two independent groups.
In order to check whether gender influences ToM performances, as is the case
with the recognition of facial expressions (Li, Yuan, & Lin, 2008), paired comparisons within the HC group (n = 26) were performed using the non-parametric
Mann–Whitney U test for two independent groups. In addition, paired comparisons
among all participants (n = 70) were performed using the parametric Student’s t-test
for two independent groups.
The p value was significant if less than 0.05.
Statistical analyses were performed using SPSS 15.0 software.
3. Results
3.1. Clinical, neuropsychological background and psychiatric
assessment (Tables 1 and 2)
A significant difference was found between the early PD group
and the advanced PD group for the H&Y and S&E scales in the
“off” dopa condition. As far as the “on” dopa conditions were concerned, no difference was found between the early PD group and
the advanced PD group for the H&Y and S&E scales (see Table 1).
No significant difference was found between either of the two
early PD groups (medicated vs. unmedicated) and the advanced
PD group for any of the neuropsychological and psychiatric tests,
except the Stroop Test and the action (verb) fluency task (see
Table 2).
No significant difference was found between the medicated
and unmedicated conditions in the early PD group for the Mattis
Dementia Rating Scale (Z = −0.3, p = .7).
3.2. Control tasks
No significant difference was found between the three groups,
i.e. the advanced PD group and the two early PD groups (medicated
vs. unmedicated,) and the HC group for any of the inclusion tests
(Benton Facial Recognition Test, Token Test and PPTT) (see Table 2).
No significant difference was found in the early PD group
between the medicated and unmedicated conditions for these
inclusion tests (Benton Facial Recognition Test: Z = −0.7, p = .4;
Token Test: Z = (0.1, p = .8, and PPTT: Z = (1.2, p = .1).
3.3. ToM tasks
Performances by the participants on the ToM tasks are shown
in Table 3.
3.3.1. Comparisons between the two parallel versions (A&B) of
each of the ToM tasks
No difference was found for any of the variables of the faux pas
recognition task between versions A and B in the HC group (p > .1
for all the comparisons).
No difference was found for the emotion attribution score of
the Reading the Mind in the Eyes test between versions A and
B in the HC group (p > .1). Note that a significant difference was
found for the control task score of the Reading the Mind in the
Eyes test (gender score) between versions A and B in the HC group
(p = .01).
3.3.2. Gender comparisons in each of the ToM tasks
No difference was found, and scores were totally comparable
between men and women in the HC group and among all participants (p > .2 for all the comparisons).
3.3.3. Faux pas recognition test (“cognitive” and “affective” verbal
ToM task)
A significant difference was found for the intention attribution
score (“cognitive” ToM score) between the early PD patient group
in the unmedicated condition, the advanced PD group and the
HC group. Paired comparisons for the intention attribution score
(“cognitive” ToM score) showed that the advanced PD group was
impaired in comparison with the early PD group in the unmedicated condition (U = 105.5, p = 0.03) and the HC group (U = 224.5,
p = 0.02). No significant difference, however, was found between
the early PD group in the unmedicated condition and the HC group
(U = 167.0, p = 0.9).
J. Péron et al. / Neuropsychologia 47 (2009) 406–414
Note that a trend towards significance was observed for the
intention attribution score (“cognitive” ToM score) between the
early PD patient group in the medicated condition, the advanced
PD group and the HC group. Paired comparisons for the intention
attribution score (“cognitive” ToM score) showed that the advanced
PD group was impaired in comparison with the HC group (U = 224.5,
p = 0.02). No significant difference, however, was found between the
advanced PD group and the early PD group in the medicated condition (U = 186.5, p = 0.3), nor between the early PD group in the
medicated condition and the HC group (U = 179.5, p = 0.3).
Additionally, a trend towards significance was observed for the
correct hits score (“cognitive” ToM score) between the early PD
patient group in the unmedicated condition, the advanced PD group
and the HC group. Paired comparisons for the correct hits score
showed that the advanced PD group was impaired in comparison
with the HC group (U = 240.5, p = 0.045). There was a trend towards a
statistically significant difference between the advanced PD group
and the early PD group in the unmedicated condition (U = 111.0,
p = 0.06). No significant difference, however, was found between
the early PD group in the unmedicated condition and HC group
(U = 165.0, p = 0.9).
A trend towards significance was observed for the explanation
score (“cognitive” ToM score) between the early PD patient group
in the unmedicated condition, the advanced PD group and the HC
group. Paired comparisons for the explanation score showed a trend
towards significant difference between the advanced PD group
and the HC group (U = 262.0, p = 0.09), and between the advanced
PD group and the early PD group in the unmedicated condition
(U = 115.5, p = 0.07). No significant difference, however, was found
between the early PD group in the unmedicated condition and the
HC group (U = 150.0, p = 0.5).
No significant difference was found between the three groups,
i.e. the early PD group (medicated/unmedicated), the advanced PD
group and the HC group, for any of the other variables of the faux
pas recognition test, including the “affective” ToM score, i.e. the
emotion attribution score.
Lastly, no significant difference was found between the medicated and unmedicated conditions in the early PD group for any
of the variables of the faux pas recognition test (correct hits score:
Z = (1.5, p = .1; correct rejects score: Z = (0.5, p = .5; correct faux pas
story control score: Z = (0.8, p = .4; correct neutral story control
score: Z = (0.4, p = .6; detection score: Z = (1.1, p = .2; explanation
score: Z = (1.5, p = .1; intention attribution score: Z = (0.9, p = .3; emotion attribution score: Z = (1.4, p = .1; total detection score: Z = (0.3,
p = .7; total control questions score: Z = (0.5, p = .5).
3.3.4. Reading the Mind in the Eyes test (“affective” visual ToM
task)
No significant difference was found between the three groups,
i.e. the early PD group (medicated/unmedicated), the advanced PD
group and the HC group, for the “affective” ToM task (Reading the
Mind in the Eyes test) (see Table 3). No significant difference was
found between the medicated and unmedicated conditions in the
early PD group for any of the variables of the Reading the Mind in
the Eyes test (gender score: Z = (0.7, p = .4; emotion score: Z = (0.1,
p = .5).
3.4. Correlations
3.4.1. Correlations between the control tasks and the ToM task
In the advanced PD group, there was a significant correlation between the PPTT score and the correct hits score (r = 0.540,
p = 0.004), the explanation score (r = 0.504, p = 0.007), and the
intention attribution score (r = 0.466, p = 0.001) of the faux pas
recognition test.
411
There was no significant correlation in the advanced PD group,
however, between the Token Test score and the correct hits score
(r = 0.104, p = 0.6), the explanation score (r = 0.190, p = 0.3), and the
intention attribution score (r = 0.972, p = 0.007) of the faux pas
recognition test.
3.4.2. Correlations between the neuropsychological background
and the ToM task
In the advanced PD group, there was no significant correlation
between the interference score of the Stroop test and either the
intention attribution score (r = 0.295, p = 0.13) or the correct hits
score of the faux pas test (r = 0.368, p = 0.59). Nevertheless, analysis
revealed that there was a significant correlation between the interference score of the Stroop test and the explanation score of the
faux pas test (r = 0.424, p < 0.02). There was no significant correlation between the action verb fluency test and either the intention
attribution score (r = 0.114, p = 0.57), the correct hits score (r = 0.261,
p = 0.18) or the explanation score of the faux pas test (r = 0.298,
p = 0.13).
4. Discussion
The aim of the present study was to clarify the possible role of
the nigrostriatal and mesolimbic dopaminergic pathways in ToM.
We compared the performances of patients with PD in the early
and advanced stages of the disease with those of HC on two ToM
tasks: a verbal one (faux pas recognition test), which is thought
to reflect both the cognitive and affective subcomponents of ToM,
and a visual one (Reading the Mind in the Eyes test), which is
thought to reflect the affective subcomponent of ToM. In addition, we compared the performances of the early PD patients with
and without DRT on the same tasks. Both the patient and the HC
groups were randomly selected and matched for age and education
level in order to avoid non specific biases. Similarly, all participants
performed normally on the tasks assessing the early processing
stages of the cognitive abilities required for each experimental
task.
Results showed that the performances by the early PD patients
on the ToM tasks were no different from those of the HC participants. Furthermore, there was no significant difference between
the medicated and unmedicated conditions in the early PD patients.
The advanced PD patients, however, displayed specific impairment
on the intention attribution score (“cognitive” ToM score) of the
faux pas recognition task and a trend towards impairment on the
explanation and corrects hits scores (“cognitive” ToM scores) of
the faux pas test. The advanced PD patients did not present any
impairment in the ToM tasks sustained by affective ToM components (emotion attribution score of the Reading the Mind in the
Eyes test and emotion attribution score of the faux pas recognition
test).
Our results could therefore suggest an absence of ToM impairment in the early stages of PD, regardless of the presence or absence
of DRT, unlike the more advanced PD patients, who did present ToM
impairment. A ToM deficit may therefore be present in PD patients
whose degenerative process has spread beyond the dopaminergic
pathways, in particular to the limbic system, unlike the early PD
patients, whose neuronal loss is thought to be restricted to the
nigrostriatal and mesolimbic dopaminergic systems (Braak et al.,
2003). In addition, our results appear to indicate that the errors
made by the advanced PD patients in the faux pas recognition task
can be ascribed to an inability to construct mental representations
(i.e. impaired “cognitive” ToM), rather than to general ToM impairment (i.e. impaired “cognitive” and “affective” ToM). Our results
seem to be in line with previous findings suggesting that cognitive
412
J. Péron et al. / Neuropsychologia 47 (2009) 406–414
and affective mentalizing abilities are partly dissociable (Brothers
and Ring, 1992; Coricelli, 2005).
There were several limitations to the present study that need to
be acknowledged and addressed.
First, the notion of ToM refers not only to the ability to represent
other people’s mental states but also to the ability to build a representation of one’s own mental states. In the present study, however,
we did not investigate all the facets of ToM because we did not test
the ability of PD patients to construct representations of their own
behaviour.
Second, the fact that early PD patients did not display any impairment at the behavioural level does not mean that these patients
used exactly the same resources to perform the task as the HC participants. It is possible to put forward the hypothesis that these
early PD patients used more resources and put more effort into this
task than their HC counterparts. This alternative explanation of our
results could be linked to reduced sensitivity to the ToM tasks we
used in the present study. The faux pas recognition task and the
Reading the Mind in the Eyes test were not developed in the context of PD, but rather to test ToM abilities in psychiatric pathologies
characterised by major social maladjustment (e.g. autism) (BaronCohen et al., 1997). If ToM deficits do indeed occur in PD, even in
the early stages of the disease, they may be less pronounced than in
autism and require extremely sensitive tasks to de detected. These
two ToM tasks also present other limitations, notably the fact that
they are not ecological. The faux pas recognition task features verbal material, and the different subprocesses required for attributing
other people’s mental states in everyday life may differ from those
required for verbal material. In futures studies, it might be interesting to include a multimodal task, as this would make it possible
to take all the sensory modalities into consideration. As far as the
Reading the Mind in the Eyes test is concerned, the main problem
arises from the poorness of the categories used in such a context.
Moreover, the recognition of mental states based on the alternatives
suggested (four in this experiment) does not necessarily correspond
to the inferences we are called upon to make (without explicitly
listed alternatives) in everyday life.
Third, even though we counterbalanced the “on” and “off” conditions in the early PD patients, and even though analysis failed
to show a significant difference between the two parallel versions
of the ToM tasks we used, the double testing may have induced a
learning effect, which may in turn have influenced our results.
Lastly, we need to bear in mind that we did not directly test
the involvement of the dopaminergic system in ToM. In humans,
it is possible to study the dopaminergic system in two ways. The
first direct way consists in reducing the dopamine level by administering neuroleptics to healthy volunteers. To our knowledge,
no published studies have investigated the impact of neuroleptics on ToM in healthy volunteers. The second way of studying
the dopaminergic system consists in using the dopaminergic
denervation model of PD. However, this model presents several
methodological limitations. First, as we have already pointed out,
it does not allow for the directly testing of the dopaminergic pathways. Second, even if the hallmark of PD is dopamine depletion
in the striatum and the mesolimbic area, thereafter other areas
(including cortical ones) gradually become affected by the disease.
At these more advanced stages of the disease, the deficits that are
observed (e.g. in ToM) can no longer be as attributed specifically to
dopaminergic depletion.
The hypothesis of an absence of ToM impairment in patients in
the early stages of PD, as opposed to more advanced PD patients,
who do present ToM impairment, would appear to be confirmed by
the results reported in the handful of studies (Mengelberg & Siegert,
2003; Mimura et al., 2006; Saltzman et al., 2000) that have already
explored ToM in PD patients. Although the patients included in
these studies were not accurately described, making it difficult to
identify the stages of the disease with any degree of accuracy, all
three studies reported ToM deficits in PD, accompanied by a major
dysexecutive syndrome. This proves that these patients were in the
advanced stages of the pathology, and the presence of a dysexecutive syndrome strongly suggests that the degenerative process had
spread beyond the dopaminergic pathways.
The first study exploring ToM in PD was published by Saltzman
et al. (2000). The authors examined ToM and its relationship to
executive functioning by administering four ToM tests and three
executive tasks to 11 non-demented patients with idiopathic PD,
8 elderly HC and 9 university-age HC. The ToM battery consisted
of two false belief stories (one first- and one second-order belief
attribution task), a Droodle task (a type of perspective task), a “spy”
model task and a deception task called the Knower/Guesser task.
The executive battery consisted of the 5-point fluency test, the California card-sorting task and the verbal fluency task. Compared
with both HC groups, PD patients obtained a significantly lower
ToM composite score (i.e. the sum of the four ToM scores) and
performed significantly worse on the false belief stories and the
“spy” model task, though not on the Knower/Guesser and Droodle tasks. As far as the executive tests were concerned, PD patients
displayed deficits on both the five-point fluency task and the verbal fluency task. Moreover, significant relationships between the
ToM measures and the executive tasks were also found. Mengelberg
and Siegert (2003) replicated these results, adding a control condition of sequencing abilities in order to avoid a specific bias. The
relationship between ToM, decision-making and executive functioning has also been examined by Mimura et al. (2006) in 18 PD
patients and 40 HC. These authors used the Iowa Gambling Task
(IGT), which assesses the ability to take profitable decisions, the
Reading the Mind in the Eyes test and a battery of executive tests
assessing set-shifting, planning and inhibition abilities, as well as
lexical availability. This study showed that PD patients performed
significantly more poorly than matched HC on the whole set of
tasks.
In our study, although the advanced PD patients did not present
a major dysexecutive syndrome, their performances on the action
(verb) fluency task, which were poorer than those of the early
PD group, would appear to confirm the impairment of executive
abilities. Whereas the tests used to assess neuropsychological background may not be sufficiently sensitive to detect early impairment,
the hypothesis of a broad cognitive deficit stemming from diffuse
brain damage (Borod, 1992; Mandal et al., 1991) can be excluded in
the case of our early PD patient group, and the absence of marked
neuropsychological dysfunction in this patient group is in favour of
neuronal loss being restricted to the dopaminergic systems.
In the three studies described above, the fact that the PD patients
displayed a dysexecutive syndrome could explain their mental state
inference deficit. In our own advanced PD patients group, we found
a significant correlation between the Stroop Interference score and
one subscore of the faux pas recognition test (explanation score).
Some authors have demonstrated double dissociations between
ToM and executive functioning by controlling for executive functions in their results (Fine et al., 2001; Gregory et al., 2002; Lough et
al., 2001; Rowe et al., 2001). Others have claimed that ToM is dependent upon executive functioning (Carlson, Moses, & Breton, 2002;
Channon & Crawford, 2000; Stuss et al., 2001). Even though the
relationship between executive functioning and ToM remains subject to debate, the ToM impairments reported in both the previous
studies and our group of advanced PD patients could be the consequence of general cognitive deterioration in the advanced stages of
the disease, rather than of a more specific dopaminergic deficit.
The discrepancy between our results and the results reported
in previous studies could be explained by the greater homogene-
J. Péron et al. / Neuropsychologia 47 (2009) 406–414
ity of our patient groups in terms of age, duration, and severity of
the disease, and mood as measured by the Montgomery–Asberg
Depression Rating Scale (MADRS, Montgomery & Asberg, 1979). In
the present study, PD patients were divided into two distinct and
homogeneous groups on the basis of disease duration and severity,
age at the time of the interviews and dopa sensitivity. The results
obtained on the H&Y and S&E scales in the “off” conditions attest
to the fact that the two groups differed in terms of disease severity.
In addition, the fact that there was no difference in the “on” dopa
conditions attests to the fact that the advanced PD patients still had
dopa sensitivity. In addition, we explored ToM in early PD patients
who either were or were not receiving DRT. It is the homogeneity of
our patient groups that allows us to infer the specific involvement of
the dopaminergic pathways in ToM. In contrast, the patients in previous studies were not accurately described. Mimura et al. (2006)
examined PD patients from a broad age range (49–76 years) and
for whom neither the duration nor the severity of the disease were
clearly reported. Mengelberg and Siegert (2003) and Saltzman et
al. (2000) studied similarly heterogeneous PD patient groups. In
Mengelberg and Siegert’s study, out of a total of 13 PD patients, 2
were in Stage 4, 6 were in Stage 3 and 4 were in Stage 2 on the H&Y
disability scale (note that the H&Y stage of the 13 patient was not
reported); their ages ranged from 50 to 84 years and their ages at
the onset of the first Parkinsonian symptoms ranged from 48 to 82
years. In Saltzmann et al.’s study, ages ranged from 48 to 84 years
and disease duration was not reported. Moreover, dopa sensitivity
remained unknown in all three studies because disability scales,
such as the H&Y scale, were not scored in “off” periods. The homogeneity of our patient groups was also controlled in terms of mood
disorders. It is now well documented that patients with depression have ToM impairments during remission from acute episodes
(Inoue, Tonooka, Yamada, & Kanba, 2004; Inoue, Yamada, & Kanba,
2006; Lee, Harkness, Sabbagh, & Jacobson, 2005). In the present
study, however, none of the PD patients reached pathological scores
on the depression scale. In Mimura et al.’s study (2006), 8 out of
18 PD patients manifested depression disorders (2 were depressed
and 6 were borderline). In Mengelberg and Siegert’s study (2003),
results showed that PD patients were significantly depressed compared with HC, while in Saltzman et al.’s study (2000), the mood
state was not even assessed. The fact that most of the PD patients
included in previous studies displayed mood disorders, including
depression, may have given rise to confounding factors, which may
have influenced the results.
In conclusion, our results do not allow us to conclude that ToM
abilities are impaired in the early stages of PD, when neuronal
loss is mainly restricted to the dopaminergic systems. Rather, like
previous studies, our results seem to indicate impairment of ToM
abilities at the stage in the disease where the degenerative process
has spread beyond the dopaminergic pathways. In addition, they
seem to suggest that advanced PD patients display deterioration in
the “cognitive” ToM component, rather than a general ToM impairment (“cognitive” and “affective” ToM), thus supporting the idea
that cognitive and affective mentalizing abilities are partly dissociable. Moreover, the fact that DRT did not influence the results of this
study suggests that the nigrostriatal and mesolimbic dopaminergic
pathways do not contribute to ToM abilities.
Acknowledgements
We would like to thank the patients and normal controls for
giving up their time to take part in this study, and the neurologists who helped us to recruit the early PD patient (in alphabetical
order: Drs V. Deburghraeve, D. Ménard, MC. Minot-Myhié, R. Murtada, H. Olivet and C. Schleich), as well as Mme Wiles-Portier for
preparing the manuscript. We would also like to express our grati-
413
tude to the “Association des Parkinsoniens d’Ille et Vilaine (APIV)”
patients’ association. This study was funded by the Neurology Unit
of Pontchaillou University Hospital, Rennes, France (Prof. G. Edan).
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