Emotional and Cognitive Social Processes Are Impaired in Parkinson's Disease and Are Related to Behavioral Disorders

Abstract

Objective:
Parkinson's disease (PD) is associated with behavioral disorders that can affect social functioning but are poorly understood. Since emotional and cognitive social processes are known to be crucial in social relationships, impairment of these processes may account for the emergence of behavioral disorders.

Method:
We used a systematic battery of tests to assess emotional processes and social cognition in PD patients and relate our findings to conventional neuropsychological data (especially behavioral disorders). Twenty-three PD patients and 46 controls (matched for age and educational level) were included in the study and underwent neuropsychological testing, including an assessment of the behavioral and cognitive components of executive function. Emotional and cognitive social processes were assessed with the Interpersonal Reactivity Index caregiver-administered questionnaire (as a measure of empathy), a facial emotion recognition task and two theory of mind (ToM) tasks.

Results:
When compared with controls, PD patients showed low levels of empathy (p = .006), impaired facial emotion recognition (which persisted after correction for perceptual abilities) (p = .001), poor performance in a second-order ToM task (p = .008) that assessed both cognitive (p = .004) and affective (p = .03) inferences and, lastly, frequent dysexecutive behavioral disorders (in over 40% of the patients). Overall, impaired emotional and cognitive social functioning was observed in 17% of patients and was related to certain cognitive dysexecutive disorders. In terms of behavioral dysexecutive disorders, social behavior disorders were related to impaired emotional and cognitive social functioning (p = .04) but were independent of cognitive impairments.

Conclusions:
Emotional and cognitive social processes were found to be impaired in Parkinson's disease. This impairment may account for the emergence of social behavioral disorders.

Full text

Emotional and Cognitive Social Processes Are Impaired in Parkinson’s
Disease and Are Related to Behavioral Disorders
Pauline Narme
Jules Verne University of Picardie and Descartes
University of Paris
Harold Mouras
Jules Verne University of Picardie
Martine Roussel
Jules Verne University of Picardie and Amiens University
Medical Center
Cécile Duru
Amiens University Medical Center
Pierre Krystkowiak and Olivier Godefroy
Jules Verne University of Picardie and Amiens University Medical Center
Objective: Parkinson’s disease (PD) is associated with behavioral disorders that can affect social functioning
but are poorly understood. Since emotional and cognitive social processes are known to be crucial in social
relationships, impairment of these processes may account for the emergence of behavioral disorders. Method:
We used a systematic battery of tests to assess emotional processes and social cognition in PD patients and
relate our findings to conventional neuropsychological data (especially behavioral disorders). Twenty-three
PD patients and 46 controls (matched for age and educational level) were included in the study and underwent
neuropsychological testing, including an assessment of the behavioral and cognitive components of executive
function. Emotional and cognitive social processes were assessed with the Interpersonal Reactivity Index
caregiver-administered questionnaire (as a measure of empathy), a facial emotion recognition task and two
theory of mind (ToM) tasks. Results: When compared with controls, PD patients showed low levels of
empathy (p⫽.006), impaired facial emotion recognition (which persisted after correction for perceptual
abilities) (p⫽.001), poor performance in a second-order ToM task (p⫽.008) that assessed both cognitive
(p⫽.004) and affective (p⫽.03) inferences and, lastly, frequent dysexecutive behavioral disorders (in over
40% of the patients). Overall, impaired emotional and cognitive social functioning was observed in 17% of
patients and was related to certain cognitive dysexecutive disorders. In terms of behavioral dysexecutive
disorders, social behavior disorders were related to impaired emotional and cognitive social functioning (p⫽
.04) but were independent of cognitive impairments. Conclusions: Emotional and cognitive social processes
were found to be impaired in Parkinson’s disease. This impairment may account for the emergence of social
behavioral disorders.
Keywords: empathy, emotion recognition, theory of mind, behavioral disorders, Parkinson’s disease
Although the motor symptoms of Parkinson’s disease (PD) are
well known, the condition is also associated with a spectrum of
general and cognitive non-motor dysfunctions (Caballol, Marti, &
Tolosa, 2007;Cronin-Golomb, 2010;McKinlay, Grace, Dalrymple-
Alford, & Roger, 2010;Whittington, Podd, & Kan, 2000), includ-
ing changes in mood and behavior in particular (Aarsland, Marsh,
& Schrag, 2009;Delgadillo-Iniguez, Corvol, Gely-Nargeot, &
Lacomblez, 2006;Levy & Dubois, 2006). Behavioral dysexecutive
disorders (BDDs) can also emerge (Godefroy et al., 2010;Mathias,
2003). A dysexecutive behavioral disorder (e.g., global hypoacti-
Pauline Narme, Laboratoire de Neurosciences Fonctionnelles et Pathologies
(EA 4559), Jules Verne University of Picardie and EquipeNeuropsychologie du
Vieillissement (EA 4468), Institute of Psychology Descartes University of Paris;
Harold Mouras, Laboratoire de Neurosciences Fonctionnelles et Pathologies (EA
4559), Jules Verne University of Picardie; Martine Roussel, Laboratoire de Neu-
rosciences Fonctionnelles et Pathologies (EA 4559), Jules Verne University of
Picardie and Département de Neurology, Amiens University Medical Center,
Amiens, France; Cécile Duru, Département de Neurology, Amiens University
Medical Center, Amiens, France; Pierre Krystkowiak and Olivier Godefroy, Labo-
ratoire de Neurosciences Fonctionnelles et Pathologies (EA 4559), Jules Verne
University of Picardie and Département de Neurology, Amiens University Med-
ical Center, Amiens, France.
This work was funded by grants from the French Ministry of Education
and Research and the Picardy Regional Council. The authors are grateful
to the psychologists F. Fourré-Renard, A. Routier, V. Tourbier, and S.
Wannepain (Neurology Department, Amiens University Medical Center)
for their contribution to the neuropsychological testing. We also thank Dr.
David Fraser (Biotech Communication, Damery, France) for improving the
manuscript’s English.
Correspondence concerning this article should be addressed to Pau-
line Narme, Equipe Neuropsychologie du Vieillissement (EA 4468),
Institut de Psychologie, Université Paris Descartes, 71 avenue Edouard
Vaillant, 92774 Boulogne-Billancourt, France. E-mail: paulinenarme@
gmail.com
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Neuropsychology © 2013 American Psychological Association
2013, Vol. 27, No. 2, 182–192 0894-4105/13/$12.00 DOI: 10.1037/a0031522
182

vity with apathy-abulia; disinterest and indifference; irritability-
impulsivity-aggressiveness; social behavior disorders and sexual,
eating, and urinary behavior disorders) is defined as one that (i)
cannot be more readily explained by perceptuomotor, psychiatric,
or other cognitive disorders, (ii) induces significant changes rela-
tive to premorbid behavior, and (iii) has a significant impact on
activities of daily living, social life, or work (Godefroy et al.,
2010). Although these behavioral symptoms can affect the pa-
tient’s autonomy (Godefroy et al., 2010), social functioning, and
quality of life (Gallagher, Lees, & Schrag, 2010;Leroi et al., 2011;
Mathias, 2003;Poewe, 2008), they remain poorly understood. In
contrast to initial suppositions, BDDs may occur in the absence of
cognitive executive dysfunction (e.g., inhibition, mental flexibi-
lity, goal setting, planning, etc.) (Eslinger & Damasio, 1985;
Godefroy, 2003). Furthermore, this dissociation appears to be
more frequent than a combined behavioral and dysexecutive cog-
nitive syndrome (Godefroy et al., 2010). These findings suggest
that BDDs cannot necessarily be explained by cognitive impair-
ments.
Emotional and cognitive social processes are known to be
crucial in social relationships. Hence, impairment of these pro-
cesses could account for behavioral disorders, as has already been
suggested in frontotemporal dementia (Gregory et al., 2002).
These emotional and cognitive social processes include empathy
(the ability to share and understand another person’s feelings;
Decety & Jackson, 2004), the ability to identify other’s emotions
(from facial cues, e.g.), and theory of mind (ToM, the ability to
infer another person’s mental states; Premack & Woodruff, 1978).
As shown by lesion studies (e.g., Shamay-Tsoory & Aharon-
Peretz, 2007) and functional studies (Hynes, Baird, & Grafton,
2006;Kalbe et al., 2010), ToM abilities can be subdivided into two
subcomponents according to the nature of the mental state: infer-
ence of beliefs or intentions (cognitive ToM) and inference of
affective states (affective ToM). Several studies have suggested
that certain emotional and cognitive social processes are altered in
PD. For example, emotional recognition impairments have been
widely reported in relation to both facial cues (e.g., Clark,
Neargarder, & Cronin-Golomb, 2008;Dujardin et al., 2004;Her-
rera, Cuetos, & Rodriguez-Ferreiro, 2011;Sprengelmeyer et al.,
2003) and auditory cues (Paulmann & Pell, 2010;Pell & Leonard,
2003;van Tricht, Smeding, Speelman, & Schmand, 2010; for a
meta-analysis, see Gray & Tickle-Degnen, 2010). More recently, a
few studies of PD patients’ ability to infer mental states have
suggested the presence of a ToM impairment (Bodden, Mollen-
hauer et al., 2010;Péron et al., 2009;Roca et al., 2010;Saltzman,
Strauss, Hunter, & Archibald, 2000; for reviews, see Bodden,
Dodel, & Kalbe, 2010 and Poletti, Enrici, Bonuccelli, & Adenzato,
2011). However, it is still unclear whether the ToM impairment
concerns both the cognitive and affective components. A recent
review has argued in favor of a specific impairment of cognitive
ToM (Poletti et al., 2011), whereas two recent clinical studies
reported an impairment of both ToM subcomponents (Bodden,
Mollenhauer et al., 2010;Tsuruya, Kobayakawa, & Kawamura,
2011). Moreover, the nature of an emotional and cognitive social
dysfunction in PD remains ill-defined. Some researchers have
suggested that ToM impairment occurs only in advanced PD and
is combined with cognitive impairments (Bodden, Mollenhauer et
al., 2010;Péron et al., 2009). However, evidence of a direct
association between BDDs on one hand and the impairment of
emotional and cognitive social processes in PD on the other is still
lacking. This issue has to be addressed through systematic assess-
ment of emotional and cognitive social processes, behavioral
changes, and cognitive impairments. To the best of our knowledge,
this type of assessment has never previously been reported.
Hence, the aims of the present study were to (i) examine
emotional and cognitive social processes in PD patients by apply-
ing a multidimensional approach (i.e., a systematic battery of
empathy, emotion recognition, and ToM tasks), (ii) explore the
relationships between emotional and cognitive social processes
and neuropsychological data, and (iii) determine whether impair-
ments in emotional and cognitive social processes are related to
BDDs (especially in the social domain). In line with previous
studies, we hypothesized that emotional and cognitive social pro-
cesses are impaired in PD patients and that these impairments are
related to one or more BDDs that cannot be accounted for by
cognitive impairments. In contrast to previous studies, we per-
formed both group comparisons and individual analyses of the
frequency of emotional and cognitive social process impairments
in PD.
Method
Participants
Twenty-three PD patients were included in the study. All had
been referred to the Neurology Department at Amiens University
Medical Center and all met the U.K. Parkinson’s Disease Society
Brain Bank criteria for idiopathic PD (Hughes, Daniel, Blankson,
& Lees, 1993). Dopaminergic depletion was confirmed by a
DaTscan
®
. The PD patients were free of other neurological or
psychiatric diseases and dementia (Emre et al., 2007) and none met
the criteria for impulse control disorders. None was receiving deep
brain stimulation. Disease severity was rated on the Unified Par-
kinson’s Disease Rating Scale (UPDRS) motor score (Fahn, Elton,
& Committee, 1987) and the Hoehn and Yahr score (Hoehn &
Yahr, 1967). Patients were tested while on medication. The pa-
tients’ demographic and clinical characteristics are summarized in
Table 1. Forty-six healthy controls (HCs, matched for age and
educational level) were also included in the study (see Table 1).
The study’s power was increased by pairing two HCs with each
patient. Statistics for groups of unequal sample sizes were used.
All patients and HCs gave their written, informed consent to
participation, and the study was approved by the local investiga-
tional review board (Comité de Protection des Personnes Nord
Ouest II, Amiens, France).
Cognitive and Behavioral Assessments
All the cognitive and behavioral assessments were performed
within 3 months of the motor assessments. A neuropsychological
battery was used to estimate global cognitive functioning (the
Mini-Mental State Examination [MMSE; Folstein, Folstein, &
McHugh, 1975] and the Mattis Dementia Rating Scale [DRS;
Mattis, 1976]), anxiety (using the Goldberg’s anxiety scale
[Goldberg, Bridges, Duncan-Jones, & Grayson, 1988]) and depres-
sion (on the Montgomery and Asberg Depression Rating Scale
[MADRS], Montgomery & Asberg, 1979). Visuoconstructive
abilities were explored with the Rey-Osterrieth Complex Figure
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183
SOCIAL COGNITION IN PARKINSON’S DISEASE

(Rey, 1959). Executive functions were assessed with validated,
French-language versions of the Trail Making Test (Reitan, 1958),
Stroop test (Stroop, 1935), Modified Card Sorting test (Nelson,
1976), and verbal fluency tests (Cardebat, Doyon, Puel, Gouet, &
Joanette, 1990). Nine cognitive indexes were specifically ana-
lyzed: the Trail Making Test A time, the Stroop naming subtest
time, the Stroop reading subtest time (all of which measure initi-
ation), the Modified Card Sorting test categories (rule deduction),
categorical and literal fluency test results (information generation),
the Stroop inhibition index (errors in the interference subtest minus
errors in the naming subtest), and perseverative errors in the
Modified Card Sorting test and Trail Making Test B (shifting).
Using normative data, participants with ⱖ3 impaired cognitive
indexes were considered to be suffering from dysexecutive cogni-
tive syndrome (Godefroy & GREFEX, 2008;Godefroy et al.,
2010).
The validated Behavioral Dysexecutive Syndrome Inventory
(BDSI; Godefroy et al., 2010) was used to explore BDDs. The
BDSI is a structured interview of an informant that assesses
changes in 12 domains (e.g., global hypoactivity with apathy-
abulia; hyperactivity-distractibility-psychomotor instability;
anosognosia-anosodiaphoria; social disorders and sexual, eating,
and urinary behavior disorders) relative to previous behavior. In a
procedure similar to that used by the Neuropsychiatric Inventory
(Cummings et al., 1994), the informant was first asked a general
screening question about a given domain. If the informant pro-
vided a positive answer, the domain was then explored in detail
with eight questions. The informant had to rate the frequency of
the disorder (1: occasional, i.e., less than once a week; 2: some-
times, about once per week; 3: frequent, several days a week but
not daily; 4: very frequent, i.e., daily) and its severity in everyday
life (1: mild; 2: moderate; 3: severe). The frequency ⫻severity
product was used as behavioral index for each domain. The do-
main was considered to be impaired when this index was greater
than 2 (Godefroy et al., 2010). With reference to normative data,
participants with ⱖ3 impaired domains were considered to be
suffering from behavioral dysexecutive syndrome (Godefroy et al.,
2010). We specifically analyzed social behavior disorders (e.g.,
“Does the patient present socially inappropriate behavior or often
act in a damaging way because he or she disregards the rules?”)
because the latter were hypothesized to be related to impaired
emotional and cognitive social processes.
Assessment of Emotional and Cognitive Social
Processes
The evaluation of social processes included tests assessing both
emotional (empathy questionnaire; facial emotion recognition)
and/or cognitive subcomponents (empathy questionnaire; both the-
ory of mind tasks). All experimental tasks were created with
E-Prime 2.0 software (Psychology Software Tools, Inc.,
Pittsburgh, PA) and presented on a touch-sensitive screen.
Empathy questionnaire. The Interpersonal Reactivity Index
(IRI) (Davis, 1983) was used as a measure of empathy. It consists
of four subscales and yields an overall empathy score. In line with
the original procedure (Davis, 1983), the IRI was administered to
HCs as a self-questionnaire. Participants were asked to tell whether
various statements inquiring thoughts and feelings in a variety of
situations (e.g., “Sometimes I don’t feel very sorry for other people
when they are having problems”) describe them well or not (on a
rating scale that ranges from does not describe me well to de-
scribes me very well). For patient groups, the IRI requires care-
givers to estimate the present level of empathy (Rankin et al.,
2006).
Facial emotion recognition. The ability to recognize facial
emotions was examined using pictures from the Ekman database
(Ekman & Friesen, 1976). Faces of 10 people expressing one of
five emotions (happiness, fear, anger, disgust, or sadness) or a
neutral expression were displayed on a screen. The six possible
responses were displayed on the lower part of the screen. Parti-
cipants were required to choose the target emotion by touching the
corresponding label. For each emotion, performance was indexed
as the number of correct responses (10 per condition; total emotion
recognition score: 60). A 20-face gender decision (i.e., man or
woman) task was used to control for impairments in facial per-
ceptive processing.
Theory of mind abilities. The Faux Pas test ascertains the
ability to identify a social “faux pas” that requires an understand-
ing of the characters’ mental states (Stone, Baron-Cohen, &
Knight, 1998). Twenty stories (10 of which featured a faux pas)
were read aloud to participants, who were then asked to indicate
whether a character had said something that they should not have
said. We awarded one point for each correctly identified faux pas
story (maximum score for “hits”: 10). When participants identified
a faux pas story, five explanatory questions were then posed
Table 1
Demographic and Clinical Characteristics of the Study Population
PD (n⫽23) HCs (n⫽46) p
ⴱ
Age (yr) 62.8 ⫾12.2 63.7 ⫾11 0.78
Gender ratio (M/F) 14/9 17/29 0.06
Education (yr) 10.7 ⫾2.97 10.9 ⫾2.2 0.81
Disease duration (yr) 5.9 ⫾5.6 —
UPDRS motor score 18.1 ⫾7.7 —
Hoehn & Yahr stage (1/1.5/2/2.5/3/4) 0/0/12/2/8/1 —
LEDD (mg) 679 ⫾482 —
Note: Data are expressed as the mean ⫾standard deviation (except for gender, where the number is quo-
ted).
ⴱ
in a t-test (except for gender ratio, to which a ␹
2
test was applied). PD ⫽Parkinson’s disease; HCs ⫽
healthy controls; M ⫽male; F ⫽female; UPDRS ⫽Unified Parkinson’s Disease Rating Scale; LEDD ⫽
Levodopa equivalent daily dose.
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184 NARME ET AL.

(maximum score: 50). One of the questions tested cognitive ToM
(was the faux pas intentional?) and another assessed affective ToM
(how did the recipient feel?). The maximum score was 10 for
questions on each type of ToM (i.e., cognitive ToM and affective
ToM). A total score (of 60 at most) was computed by adding the
number of hits to the explanation score. Lastly, the subject’s
understanding was checked with two additional questions for each
faux pas story and control story (maximum score: 40).
A modified French-language version of the “Yoni” task
(Shamay-Tsoory & Aharon-Peretz, 2007) was also administered.
This task has already been used with PD patients (Bodden,
Mollenhauer et al., 2010). Fifty-four on-screen trials consisted of
Yoni’s face surrounded by four pictures (e.g., animals, fruits, or
faces). By assessing Yoni’s gaze and facial expression, partici-
pants had to complete a sentence by choosing the picture to which
the character was referring. There were two ToM-based conditions
(to test cognitive ToM [“Yoni is thinking of . . .”] and affective
ToM [“Yoni likes . . .”]) and a control condition requiring the
analysis of physical attributes. The items also differed in complex-
ity, with first-order and second-order inferences (e.g., for cognitive
ToM: “Yoni is thinking of the car that . . . wants”). Accuracy was
recorded for all items.
Statistical Analyses
Intergroup comparisons were performed using a ttest or an
analysis of variance (ANOVA) with repeated measures with group
(PD, HC) as the between-subjects factor and condition as the
within-subject factor. To control for a possible effect of depression
and anxiety, these analyses were repeated with the MADRS and
anxiety scores as covariates. We also checked that statistical find-
ings survived nonparametric analyses. For each test, neuropsycho-
logical data were compared with normative scores.
Given that (i) intergroup differences in mean values do not
necessarily imply that impairment is reliably detectable at the
individual level and (ii) knowledge of the frequency of impairment
is important for clinical purposes, performance in emotional and
cognitive social tasks was also compared with normative data
obtained from a larger HC population (n⫽100, unpublished data).
This HC population (25 males and 75 females; mean age: 62 ⫾1;
mean number of years in full-time education: 12.4 ⫾0.3) did not
differ significantly from our sample of PD patients in terms of
gender, age, or educational levels (all ps⬎.05). Impairment was
defined as performance below a cutoff at the 5% percentile. The
frequencies of emotional and cognitive social impairment in the
two groups were compared using Fisher’s exact test. An emotional
and cognitive social index was computed by adding together the
impairments observed for the emotion recognition, Yoni second-
order and the total faux pas scores (we recorded one point when-
ever the patient scored below the fifth percentile of the normative
data, leading to a maximum of three points when performance in
these three emotional and cognitive social tasks was impaired).
Lastly, correlations between the emotional and cognitive social
index and clinical features (UPDRS score, disease duration and
levodopa equivalent daily dose [LEDD]) on one hand and BDDs
on the other were analyzed using Pearson’s test. We first checked
whether or not the emotional and cognitive social index and
cognitive impairments were correlated. Analyses were performed
using SPSS software (Version 13.0, IBM Inc., Chicago, IL);
pvalues ⬍0.05 were considered to be statistically significant.
Results
Cognitive and Behavioral Assessment
Neuropsychological data are summarized in Table 2. The PD
patients differed significantly from HCs in terms of global effi-
ciency (as assessed by the MMSE and the DRS), anxiety, and
depression (see Table 2). The patients’ neuropsychological profile
was characterized by visuoconstructive difficulties, impaired inhi-
bition (as suggested by the proportion of patients with an impaired
Stroop inhibition index), and difficulties in rule deduction (as
assessed by the proportion of patients with an impaired “number of
categories” score in the Modified Card Sorting Test). Few patients
were impaired in information generation (fluency tests), initiation
(Trail Making Test A time), or shifting (perseverative errors in the
Trail Making Test B and Modified Card Sorting Test; see Table 2).
Dysexecutive cognitive disorders were relatively rare, since only
26% of patients were found to suffer from dysexecutive cognitive
syndrome. In terms of BDDs, PD patients frequently showed not
only global hypoactivity with apathy-abulia but also hyperactivity-
distractibility-psychomotor instability; stereotyped and persevera-
tive behavior; difficulties in anticipation, planning, and initiation
of activities; and disinterest and indifference (see Table 2). More
than 40% of our PD sample met the criteria for behavioral dysex-
ecutive syndrome.
Empathy Questionnaire
The overall IRI score was significantly lower in PD patients
(53.1 ⫾12.9) than in HCs (62.3 ⫾11.4; p⫽.006), suggesting
lower levels of empathy in PD.
Facial Emotion Recognition
Relative to HCs, the PD patients displayed lower accuracy (p⫽
.02) than HCs in the gender task (19.74 ⫾0.61 and 19.09 ⫾1.24,
respectively). We therefore performed a repeated measures anal-
ysis of covariance (ANCOVA) with emotion (fear, anger, disgust,
neutral, sadness, and happiness) and group (PD, HC) as between-
subjects factors and accuracy in the gender task as a covariate. The
ANCOVA revealed (i) a main effect of group (F(1) ⫽11.7; p⫽
.001), due to worse performance in PD patients than in HCs
(7.63 ⫾0.2 and 8.6 ⫾0.14, respectively); (ii) the lack of a
significant effect of emotion (p⫽.08), and (iii) a group ⫻emotion
interaction (F(5, 62) ⫽4.3; p⫽.002), due to worse performance
in PD patients than HCs for fear (6.65 ⫾2.5 and 8.9 ⫾1.47,
respectively; p⬍.001), sadness (6.83 ⫾2.59 and 7.96 ⫾1.81,
respectively; p⫽.029), and neutral expressions (8.1 ⫾1.9 and
8.93 ⫾0.98, respectively; p⫽.015) (see Figure 1). These findings
indicated that fear and sadness recognition was impaired in the PD
patients.
Theory of Mind Abilities
The “faux pas test”. A one-way ANOVA indicated lower
scores in the PD patients than in HCs for the total composite score
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185
SOCIAL COGNITION IN PARKINSON’S DISEASE

(F(1) ⫽10.76; p⫽.002) and the explanation score (F(1) ⫽11.97;
p⫽.001) (see Table 3). Aspects related to cognitive and affective
inferences were also impaired in PD (cognitive ToM score: F(1) ⫽
7.32; p⫽.009; affective ToM score: F(1) ⫽5.04; p⫽.028).
However, PD patients also had a lower comprehension score than
HCs (F(1) ⫽35.12; p⬍.001), suggesting that this result might be
due to the impairment of non-empathic processes. This interpre-
tation was supported by the results of an ANCOVA using the
comprehension score as a covariate (see Table 3), since the inter-
group differences disappeared after correcting for impaired under-
standing. Hence, these findings indicate that the PD patients’ poor
results in the faux pas task were attributable to impaired under-
standing.
The Yoni task. An ANOVA with repeated measures on order
(first, second) and condition (cognitive, affective, physical), and
with group (PD, HC) as between-subjects factor revealed (i) a
main group effect (F(1) ⫽6.06; p⫽.02), with lower scores in the
PD group (83.2 ⫾1.5) than in the HC group (88.6 ⫾1.1); (ii) a
significant effect of order (F(1) ⫽87.673; p⬍.001), due to lower
scores for second-order inferences (75.8 ⫾1.6) than first-order
inferences (95.97 ⫾0.8); and (iii) a significant group ⫻order
interaction (F(1, 66) ⫽7.49; p⫽.008), due to worse performance
in PD patients than HCs for second-order inferences. In order
to specify the effect of affective and cognitive inferences within
second-order ToM abilities, the affective, cognitive, and control
subscale scores were analyzed in a one-way ANOVA. This
showed that PD patients had lower scores than HCs for both
cognitive (62.7 ⫾4.2 vs. 76.8 ⫾2.9; F(1) ⫽8.66; p⫽.004) and
affective ToM (70.3 ⫾3.7 vs. 79.2 ⫾2.6; F(1) ⫽5.08; p⫽.03)
but not for the control condition (F(1) ⫽1.91; p⫽.18, see Figure
2). This finding suggests that both cognitive and affective second-
order ToM abilities were impaired in PD. A further ANCOVA was
performed with the DRS score as covariate. The result was not
statistically significant, suggesting that ToM impairment on the
Yoni task is not attributable to cognitive status.
Frequencies of Emotional and Cognitive Social
Impairments
The following impairments were significantly more frequent in
PD patients than in HCs: (i) the overall IRI score (29% and 6.5%
of the individuals, respectively; p⫽.03); (ii) total emotion rec-
ognition score (30.5% vs. 6.5% in the PD and HC groups, respec-
tively; p⫽.01, after the exclusion of patients impaired in the
Table 2
Neuropsychological Characteristics of the Study Population
PD (n⫽23) HCs (n⫽46) p
ⴱ
MMSE 26.3 ⫾2.5 27.6 ⫾1.7 0.014
DRS 135.4 ⫾6.3 139.5 ⫾3 0.006
MADRS 9 ⫾6.9 3.5 ⫾4 0.002
Goldberg’s Anxiety scale 3.9 ⫾2.7 1.3 ⫾1.7 ⬍0.001
Rey-Osterrieth Complex Figure task 31.2 ⫾5.3 (27%) —
Trail Making Test–Part A
Time 56 ⫾19 (4%) —
Errors 0.04 ⫾0.2 (0%) —
Trail Making Test–Part B
Time 169 ⫾99 (26%) —
Errors 0.8 ⫾1.2 (9%) —
Modified Card Sorting Test
Categories 4.3 ⫾1.7 (26%) —
Perseverative errors 4.3 ⫾3.8 (9%) —
Categorical fluency test (animals) 23 ⫾6.9 (14%) —
Letter fluency test (letter ‘P’) 14.5 ⫾6.6 (14%) —
Stroop Interference index
Time 85.7 ⫾62.4 (9%) —
Errors 3 ⫾4.8 (30%) —
Cognitive dysexecutive syndrome 26% —
BDSI
Global hypoactivity (apathy-abulia) 44% —
Anticipation-planning-initiation 39% —
Disinterest and indifference 33% —
Hyperactivity-distractibility-psychomotor instability 44% —
Irritability-impulsivity-aggressiveness 28% —
Euphoria, emotional lability, and moria 28% —
Stereotyped and perseverative behavior 39% —
Environmental dependency 0% —
Anosognosia-anosodiaphoria 11% —
Spontaneous confabulations 0% —
Social behavior disorders 17% —
Sexual or eating behavior disorders 22% —
Behavioral dysexecutive syndrome 44% —
Note: Data are expressed as the mean ⫾standard deviation or the frequency of impairment (percentage).
ⴱ
t-test. PD ⫽patients with Parkinson’s disease;
HCs ⫽healthy controls; MMSE ⫽Mini-Mental State Examination; DRS ⫽Dementia Rating Scale; MADRS ⫽Montgomery and Asberg Depression
Rating Scale; BDSI ⫽Behavioral Dysexecutive Syndrome Inventory.
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186 NARME ET AL.

gender discrimination task); (iii) the Yoni second-order score for
cognitive ToM (30.5% vs. 6.5%, respectively; p⫽.01); and for
affective ToM (17.5% vs. 2.2%, respectively; p⫽.04).
Lastly, the emotional and cognitive social index was more
frequently impaired in PD patients (4 out of 23 patients, 17.5%)
than in HCs (0 out of 46, 0%; p⫽.01). To ensure that the
impairment could not be explained by confounding factors (e.g.,
depression and cognitive status), further individual analyses were
performed. Impairment in the emotional and cognitive social index
remained significantly more frequent in the PD patients, after
exclusion of subjects meeting the criteria for moderate depression
(Montgomery & Asberg, 1979) (19% vs. 0% in the PD and HC
groups, respectively; p⫽.008) and those with global cognitive
efficiency scores close to the cutoff value (Folstein et al., 1975;
Mattis, 1976) (16% vs. 0%, respectively; p⫽.02).
Relationships With Clinical and Neuropsychological
Data
We next tested for correlations between the emotional and
cognitive social index (coded as 0: preserved; 1: impaired) on one
hand and the clinical data (UPDRS motor score, disease duration,
dopamine equivalent dose), the neuropsychological data (0: pre-
served; 1: impaired), and BDDs (0: absent; 1: present) on the other.
The emotional and cognitive social index was not correlated with
the clinical data (all ps⬎.1). Accordingly, three patients with a
poor emotional and cognitive social index had moderately severe
disease (Hoehn-Yahr stage ⫽2). The correlation analysis for the
emotional and cognitive social index and neuropsychological data
revealed: (i) no correlation with cognitive performance, other than
with some executive indexes (such as the Trail Making Test A
time, categorical fluency and the mean number of perseverative
errors in the Modified Card Sorting test; Table 4); (ii) the absence
of significant correlation with the presence of behavioral dysex-
ecutive syndrome (present in 44% of the PD patients); (iii) a
significant correlation between the emotional and cognitive social
index and social behavior disorders (see Table 4). Lastly, these
social behavior disorders were not correlated with cognitive in-
dexes, including executive disorders (see Table 4).
Discussion
Our findings can be summarized as follows: (i) PD was asso-
ciated with impairments of emotional and cognitive social pro-
cesses, as shown by lower empathy and impaired facial emotion
recognition and second-order ToM abilities (relative to HCs); (ii)
both cognitive and affective ToM inferences were impaired in PD;
(iii) the emotional and cognitive social index was correlated with
certain executive disorders (information generation and shifting);
(iv) dysexecutive behavioral syndrome was frequently observed
(in 44% of the PD patients); and (v) BDDs in the social domain
were correlated with the impairment of emotional and cognitive
social processes but not cognitive disorders (including executive
disorders).
Various impairments of emotional and cognitive social pro-
cesses have been separately reported in PD patients; these include
emotion recognition (Gray & Tickle-Degnen, 2010) and ToM
abilities (Bodden, Mollenhauer et al., 2010;Péron et al., 2009;
Poletti et al., 2011;Tsuruya et al., 2011). It has been suggested that
these impairments are due to dysfunction of the amygdala and
frontostriatal limbic circuitry in PD (Ouchi et al., 1999). In the
present study, empathy (as assessed by caregivers in the IRI) was
low in PD. However, one must also consider potentially artifactual
reductions in empathy in the context of our study. Indeed, care-
givers may have had difficulty in accurately evaluating empathy
because patients tend to present less emotional expressions (e.g.,
hypomimia). Our results also showed that the recognition of neg-
ative emotions (such as fear and sadness) was prominently im-
paired in PD patients, as has been reported elsewhere (Gray &
Tickle-Degnen, 2010). However, our study further indicates that
these difficulties persisted after correction for perceptive disorders,
Table 3
Theory of Mind Abilities Assessed in the “Faux Pas” Test
PD (n⫽23) HCs (n⫽46) pvalues
a
pcovariate
b
Hits (/10) 8.43 ⫾0.3 9.04 ⫾0.21 0.1 0.41
Explanation (/50) 30.61 ⫾1.49 36.8 ⫾1.06 0.001 0.11
Composite score (/60) 39.04 ⫾1.99 45.85 ⫾1.15 0.002 0.13
Cognitive ToM (/10) 6.04 ⫾0.35 7.22 ⫾0.25 0.009 0.48
Affective ToM (/10) 7.04 ⫾0.4 8.11 ⫾0.29 0.028 0.09
Understanding (/40) 36.56 ⫾0.3 38.69 ⫾0.2 ⬍0.001 —
Note: Data are expressed as the mean ⫾standard deviation.
a
Intergroup difference in an analysis of variance.
b
in an analysis of covariance, with the “understanding” score
as a covariate. PD ⫽Parkinson’s disease; HCs ⫽healthy controls; ToM ⫽theory of mind.
Figure 1. Facial recognition for each of six emotions, quoted as the mean
number of correct answers and the standard deviation. PD: Parkinson’s
disease; HC: healthy controls.
ⴱ
p⬍0.05
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187
SOCIAL COGNITION IN PARKINSON’S DISEASE

which could otherwise have accounted for impairments in emotion
identification (Narme, Bonnet, Dubois, & Chaby, 2011). In terms
of ToM abilities, the apparent impairment in the faux pas task did
not survive an adjustment for general understanding of the stories
and, hence, cannot be attributed to impaired ToM. Nevertheless,
poor second-order Yoni performance revealed that both cognitive
and affective ToM subcomponents were altered in our PD patients.
This contrasts with previous reports of specific impairments in
cognitive ToM (Péron et al., 2009;Poletti et al., 2011;Roca et al.,
2010) but supports recent reports of an alteration of both kinds of
inference (Bodden, Mollenhauer et al., 2010;Tsuruya et al., 2011;
Santangelo et al., 2012). These discrepancies might be explained
by assessments of patients at different stages of the disease. As
previously hypothesized, cognitive ToM impairments may precede
affective ToM impairments in the course of PD, as the brain
lesions spread from the dorsolateral to the ventromedial prefrontal
cortices (see Bodden, Dodel et al., 2010). It is noteworthy that all
our emotional and cognitive social tasks measure aspects of cog-
nition that are conceptually associated with (or may underpin)
empathy (Shamay-Tsoory, Aharon-Peretz, & Perry, 2009). For
example, accurate interpretation of the emotional meaning of an-
other person’s facial expressions and ToM abilities are important
preconditions for empathy. Taken as a whole, our results (i)
suggest the existence of altered emotional and cognitive social
processes, (ii) are coherent with caregivers’ assessment of empathy
(according to the IRI), and thus (iii) argue against the presence of
artifacts. Although our results suggest that emotional and cognitive
social processes are impaired in PD, future research will have to
confirm direct relationships between facial emotion recognition or
ToM abilities and empathy in both HCs and patients.
In contrast to previous studies, we used a structured, multidi-
mensional approach to relate impairments in emotional and cog-
nitive social processes to clinical and neuropsychological data in
general and behavioral and cognitive dysexecutive disorders in
particular (Godefroy et al., 2010). First, the emotional and cogni-
tive social index was found not to be related to clinical data or
dopaminergic medication levels; this indicates that impairments in
emotional and cognitive social processes can even appear in early
stage disease (as also suggested by Roca et al., 2010). The rela-
tionship between emotional and cognitive social dysfunction and
“standard” neuropsychological assessments has rarely been inves-
tigated in PD. Here, PD patients exhibited neuropsychological
impairments, as characterized by visuoconstructive difficulties and
impairments in certain executive processes (such as inhibition and
rule deduction). This cognitive profile is consistent with previous
reports on non-demented PD sufferers (Crucian & Okun, 2003;
Godefroy et al., 2010;Obeso et al., 2011; see Kudlicka, Clare, &
Hindle, 2011 for a review). Second, the impaired emotional and
cognitive social index was correlated with information generation
and shifting abilities. Previous research has not greatly investi-
gated the extent to which executive disorders may be related to
impairments in emotion recognition (for a meta-analysis, see Gray
& Tickle-Degnen, 2010) or ToM. In terms of facial emotion
recognition, a recent study showed that the impairments reported
in PD can be related to impairments in many neuropsychological
domains, including verbal fluency (Assogna et al., 2010). Never-
theless, impaired facial emotion recognition persists after control-
ling for cognitive disorders (Herrera et al., 2011). Whereas some
data show a correlation between impaired ToM and executive
disorders in PD (Péron et al., 2009;Saltzman et al., 2000;Santan-
gelo et al., 2012), there is also evidence to suggest that ToM
impairments can appear in the absence of executive disorders
(Bodden, Mollenhaueret al., 2010), especially in the early stages of
the disease (Roca et al., 2010; see Freedman & Stuss, 2011 for a
Figure 2. Yoni task: Cognitive and affective theory of mind (ToM). Mean accuracy (percentage) and standard
deviation according to the order and condition (cognitive, affective, control condition). PD: Parkinson’s disease;
HC: healthy controls.
ⴱ
p⬍0.05.
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188 NARME ET AL.

review). Taken as a whole, these results corroborate the notion of
functional independence between social processes and executive
cognitive functioning (see Fine, Lumsden, & Blair, 2001). Never-
theless, future research will have to examine how and when these
respective disorders can be interrelated. To this end, it would have
been interesting to perform the executive tests on the HCs.
Lastly, we looked at whether impaired emotional and cognitive
social processes and/or cognitive disorders could account for
BDDs in general and social behavior disorders in particular. We
found that behavioral dysexecutive syndrome (which is rarely
investigated in PD) was frequent, since it affected 44% of our
patients (Mathias, 2003;Godefroy et al., 2010). This relatively
high frequency and the previously reported relationship between
behavioral dysexecutive syndrome and the loss of autonomy (Go-
defroy et al., 2010) suggest that PD patients should be systemati-
cally screened for BDDs. Second, our results showed that social
behavior disorders were not related to dysexecutive cognitive
disorders (observed in about a fifth of our PD patients). This result
confirms that these two dysexecutive syndromes may be dissoci-
ated (Godefroy et al., 2010) and supports the hypothesis whereby
BDDs cannot always be explained by cognitive disorders. Accord-
ingly, neuropsychological studies have reported (i) prominent cog-
nitive dysexecutive disorders in subjects with dorsolateral lesions
and (ii) prominent BDDs in subjects with mediofrontal lesions
(Eslinger & Damasio, 1985;Blair & Cipolotti, 2000; for a review,
see Stuss, 2011). This finding also emphasizes the importance of
assessing BDDs in PD patients with otherwise intact cognitive
abilities.
In contrast, we found that social behavior disorders were related
to impairment of the emotional and cognitive social index. Ac-
cordingly, a recent study showed that impaired ToM abilities in PD
were related to the severity of apathy and behavioral disturbances
(Santangelo et al., 2011). These results are consistent with the
observation of BDDs after lesion to mediofrontal and orbitofrontal
areas of the brain— both of which are involved in emotional and
cognitive social processes (Zald & Andreotti, 2010), and become
damaged in PD (see Poletti & Bonuccelli, 2012 for a review).
Taken as a whole, these results indicate that impaired emotional
and cognitive social processes in PD have social consequences
and, thus, emphasize the need to assess these processes in routine
clinical practice.
In summary, we found that emotional and cognitive social
processes are impaired in PD and that these impairments are
related to social behavioral disorders. However, a number of study
limitations have to be addressed. First, there was a difference
(albeit not statistically significant) in gender distribution between
the two study groups, with a greater proportion of women among
the HCs. Indeed, women often show superior performance levels
in social– cognitive tasks (e.g., Derntl et al., 2010) and the potential
presence of gender bias might explain why PD patients were found
to be more frequently impaired in these tasks. Second, the study
patients had undergone a DaTscan but not an MRI scan. We cannot
rule out the possibility that periventricular and subcortical/cortical
white-matter abnormalities (rather than disease-specific lesions)
were associated with the observed impairments in emotional and
cognitive social processes. Lastly, more research on the influence
of dopaminergic therapy (e.g., the duration of treatment and the
use of levodopa vs. dopamine agonists) is needed. It would be
particularly interesting to test patients under both “on-drug” and
Table 4
Correlations Between the Various Neuropsychological Impairments on One Hand and the Emotional and Social Cognitive Index (A) and Social Behavior Disorders (B) on
the Other
Impaired MMSE DRS MADRS Anxiety Rey CDS
TMT A
time
TMT B
errors
MCST
categories
MSCT
errors
Literal
fluency
Categorical
fluency
Stroop
inhibition
index BDS
Social
behavior
(A) Emotional and social cognitive index .39 ⫺.01 ⫺.14 –.25 –.02 .25 .47
ⴱ
–.14 .25 .67
ⴱⴱ
.16 .50
ⴱ
.19 .06 .48
ⴱ
(B) Social behavior .12 .39 –.16 –.20 .38 .39 –.11 .32 .06 .31 .31 .19 .39 .50 1
Note: MMSE ⫽Mini-Mental State Examination; DRS ⫽Dementia Rating Scale; MADRS ⫽Montgomery and Asberg Depression Rating Scale; CDS ⫽Cognitive Dysexecutive Syndrome; TMT
⫽Trail Making Test; MCST ⫽Modified Card Sorting Test; BDS ⫽Behavioral Dysexecutive Syndrome.
ⴱ
p⬍.05.
ⴱⴱ
p⬍.01.
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189
SOCIAL COGNITION IN PARKINSON’S DISEASE

“off-drug” conditions in order to control for levodopa-induced side
effects and establish whether or not emotional and cognitive social
impairments are associated with dopamine depletion itself or some
aspect of dopaminergic therapy (e.g., overdoses). It would also be
valuable to explore the effect of medication class by taking the
influence of dopamine agonists into account. The latter medica-
tions have been linked to a higher incidence of impulse control
disorders (Weintraub, 2008). Although patients with impulse con-
trol disorders were excluded from the present study, some parti-
cipants were taking dopamine agonists. However, two of the four
patients with an impaired emotional and cognitive social index
were not taking dopamine agonists; this indicates that the admin-
istration of dopamine agonists is not a sufficient condition for
emotional and cognitive social impairment. Patients with impulse
control disorders demonstrate a bias toward risky choices (Voon et
al., 2011); this tendency may also extend to their interpersonal
relationships. Hence, it would be interesting to look at whether (i)
patients with impulse control disorders perform worse in social–
cognitive tasks and (ii) there is an association between their
performance and the dose of dopamine agonists.
In conclusion, the present study has practical implications for
the care of PD patients (because it emphasizes the importance of
assessing emotional and cognitive social processes) and theoretical
implications concerning our understanding of how BDDs arise.
Although our results also provide further support for a putative
role for subcortical structures and frontostriatal circuits in emo-
tional and cognitive social processes, the relationships between
impaired emotional and cognitive social functioning and subcor-
tical/cortical white-matter abnormalities merit direct investigation.
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Received June 11, 2012
Revision received November 21, 2012
Accepted December 6, 2012 䡲
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192 NARME ET AL.