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(EM 425), University of Rennes 1, Ho pital Pontchaillou, CHU de Rennes, Rennes, France
nit, Ho pital Pontchaillou, CHU de Rennes, Rennes, France
Department of Psychology and Swiss Center for Affective Sciences, University of Geneva, Geneva, Switzerland
Department, Euge` ne Marquis AntiCancer Centre, Rennes, France
ent review, we begin by providing a synopsis of the emotional disturbances observed in Parkinsons disease. We then discuss the functional roles of the striato-thalamo- cortical and mesolimbic circuits, ending with
Key Words: amygdala; basal ganglia; emotion; Par- kinsons disease
-----------------------------------------------------------*Correspondence to: Dr. Julie Pe ron, CISA, 7 rue des Battoirs, 1205
Gene` ve, Suisse; julie.peron@unige.ch
Funding agencies: Neurology Unit of Pontchaillou University Hospital in Rennes, France (Prof. G. Edan).
Relevant conflicts of interest/financial disclosures: Nothing to report. Full financial disclosures and author roles may be found in the online version of this article.
Received: 26 April 2011; Revised: 30 September 2011; Accepted: 12
October 2011
Published online 9 December 2011 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/mds.24025
This article first published online ahead of print on 9 December 2011. The article has since been updated.
EMOTION
A ND
PD
We conducted a detailed search of the literature, with the aim of reviewing all the relevant papers on emotional processing and PD. The data
Emotional Processing in PD
Researchers have reported deficits in several emo- tional components and processes in PD patients. These include not only changes in the em
ger the eye-blink startle reflex (measured using electro- myography) during stimulus presentation. Results showed that the startle reflex was s
emotional processing and notably the triggering of fear responses.13
The question of whether this reduced reactivity to emotional stimuli is driven by diminished reactivity to fear-eliciting stimuli as opposed to
These studies therefore seem to point to modifica- tions in both the subjective feeling and physiologi- cal arousal emotional component
Movement Disorders, Vol. 27, No. 2, 2012
187
TABLE 1. Overview of the clinical reports discussed in section 1 addressing the question of emotional processing in PD
Disease duration
Authors
Cognitive assessment
Dopa
Control task
Depression
Anxiety
Emotional stimuli
Dependent variables
23 PD; 17 HC
Yes
Yes
Yes
No
Hillier et al.14
8 PD; 15 HC
Yes
No
No
No
(2007)
Miller et al.15
(2009)
24 PD; 24 HC
Yes
Yes
Yes
No
Yes
(2008)
Beatty et al.19 (1989)
43 PD; 27 HC
4.7 6 NA years
(mean 6 SD)
Yes (exc.
1)
Static faces: A, D,
F, H, Neu, Sa,
Categorization
No
HC; control task: PD
< HC
Categorization and matching: PD < HC
Discrimination and
Prosopagnosia, global
efficiency, education ()
No
No
Blonder et al.20
21 PD; 17 HC
NA
(1989)
20 PD; 21 HC
Borod et al.21
(1990)
Breitenstein et al.22 (1998)
7 H&Y I; 7
H&Y II PD; 12 HC
NA
No
Static pictures:
Arousal (Likert); valence
EMG; startl
Neg, Pos, Neu
(Likert)
response
HC; eye blink: PD
< HC
Yes
Emotional words:
Arousal (Likert); valence
No
Neg, Pos, Neu
(Likert)
<
No
Static pictures:
Arousal (Likert); Valence
Startle eye bli
Neg, Pos, Neu
(Likert)
<H
Static pictures:
Static faces: A, D,
Yes
Yes
Yes
No
Yes
Static faces: A, D,
F, H, Neu, Sa
Categorization: PD <
Yes
No
No
No
Yes
Yes
No
No
No
No
S
Static faces: H, Sa,
A, F, D, Neu
Static faces: A, D,
44.0 6 28.9
months (I); 62.4
6 29.5 months
(II) (mean 6
SD)
F, H, Neu, Sa,
S
Yes
Yes
No
No
Yes
Static faces: H, Sa,
A, F, Neu
categorization
Discrimination; categorization
REP; intermodal
emotional task
categorization: PD
< HC
Discrimination and
No categorization: Stage
II PD < HC;
discrimination and categorization: stage I PD HC
Caekebeke
et al.23 (1991)
21 PD; 14 HC
5.5 6 NA years
(mean 6 SD)
Yes
Yes
No
No
No
NA
PEP/REP
Speech, RFE, REP: PD
No
HC; PEP: PD<HC
Clark et al.24 (2008)
20 PD; 23 HC
7.3 6 4.2 years
(mean 6 SD)
Yes
Yes
Yes
Yes
Yes
Static faces: A, D,
F, A, Neu., Sa., S
Categorization
REP; interpersonal
problem
Categorization: PD <
HC
Depression anxiety ()
(PD); depression anxiety (ns) (HC);
sociodemographic, clinical, cognitive (ns)
Dewick et al.25 (1991)
18 PD; 18 HC
6.0 6 NA years
(mean 6 SD)
Yes
Yes
Yes
No
Yes
Static faces: H,
Sa., A
Discrimination
No
Discrimination: PD
HC; control task: PD
< HC
Cognitive, visuospatial,
clinical (ns) (PD)
Dujardin et al.26 (2004)
18 PD; 18 HC
11.3 6 4.7 years
(mean 6 SD)
No
Yes
Yes
Yes
No
Static faces: A, Sa,
D, Neu
Categorization; intensity
(Likert)
No
Categorization and
intensity: PD < HC
Motor, executive
functions, depression, anxiety, visuospatial (ns)
NA
Speech production;
TABLE 1. (Continued)
Disease
Cognitive
Control
Authors
duration
Dopa
assessment
Depression
Anxiety
task
Emotional stimuli
Dependent variables
Haeske-Dewick
13 early PD/
Yes
Yes
Yes
No
Yes
Static faces: H,
Discrimination
et al.27
13 HC; 13
(1996)
advanced
PD/13 HC
4.9 years
(advanced) (mean 6 SD)
HC; control task:
early PD < HC;
advanced PD < HC
Jacobs et al.28 (1995)
12 PD; 30 HC
NA
(early); 8.3 6
Yes
Sa., A
Yes
Yes
No
Yes
Static faces: H, A,
on
Sa, F, Neu
Discrimination; matching
No
Discrimination and
matching: PD < HC
Cognitive, clinical,
visuospatial, depression (ns) (PD)
Kan et al.29 (2002)
Lawrence
et al.30 (2007)
16 PD; 24 HC
NA
Yes
Yes
Yes
No
Yes
Moving and static
faces: A, F, H, S, Sa, D
17 PD; 21 HC
NA
Yes
Yes
Yes
No
Yes
Static faces: A, F,
H, S, Sa, D
REP/recognition of
emotions from verbal stimuli
Categorization
Tridimensional personality questionnaire
PD < HC (F, D)
PD < HC (A)
Sociodemographic,
clinical, cognitive (ns)
Prosopagnosia (); motor, depression (ns); personality
anger score ()
Lotze et al.31 (2009)
10 PD; 10 HC
12.8 6 4.1 years
(mean 6 SD)
Yes/(OFFPET)
Yes
Yes
No
No
Dynamic emotional
and nonemotional gestures (faces and upper half of
the body)
Categorization; valence
(analogical scale)
fMRI; 11C-PET
PD < HC (recognition of emotional gesture);
PD HC (valence); PD: decrease in the L ventrolateral prefrontal cortex and the R temporal sulcus related to emotional gestures
Striatal dopamine
transporter and errors in recognition of emotional gesture (-); striatal dopa- mine transporter and activation in the left ventrolateral cortex ()
Madeley et al.32 (1995)
9 PD; 9 HC
NA
Yes
No
Yes
Yes
Yes
Normal and PD
static faces: Sa, A, D, Neu
Discrimination;
categorization; expressivity (Likert)
PFE
Categorization, discrimiNo
nation: PD HC; PD faces less expressive than normal faces
Pell and
Leonard33 (2005)
21 PD; 21 HC
3.9 6 1.9 years
(mean 6 SD)
Yes (exc.
1)
Yes
Yes
No
Yes
Static faces:
pleasant, S, H, Sa, A, D
Discrimination;
categorization; intensity (Likert)
Recognition of
emotions from verbal stimuli; REP
Discrimination,
categorization, and intensity: PD HC
Motor, severity (-)
Sprengelmeyer
et al.34 (2003)
16 PD (off);
20 PD (on);
20 HC
3.0 6 2.6 years
(off dopa); 9.3
6 4.6 years (on dopa) (mean 6 SD)
Yes/No
Yes
Yes
No
Yes
Static faces: A, F,
H, S, Sa, D
Categorization
No
on PD < HC; off PD <
No
HC (greater deficit in off dopa for A, and D)
Suzuki et al.35 (2006)
Tessitore et al.36 (2002)
14 PD; 39 HC
4.8 6 1.0 years
(mean 6 SD)
on
Yes
Yes
Yes
No
H, S, Sa, D
Categorization; intensity
(Likert)
No
Categorization and intensity: PD < HC (D)
Sociodemographic,
cognitive, depression (ns) (PD)
10 PD; 10 HC
NA
Yes/No
Yip et al.37
56 bilateral
7.2 6 4.0 years
Yes
Yes
No
No
Discrimination;
the off dopa/partially
restored in on dopa condition; RT: PD HC
REP
Discrimination and
Clinical (ns); visuospatial
(2003)
PD; 8 R
(bilateral PD);
PD; 64 HC
2.8 6 1.6
years (R PD)
(mean 6 SD)
Yes
Static faces: A, F,
No
No
No
No
Yes
Static faces: A, F
Matching
A, S, D, F categorization
Yoshimura
et al.38 (2005)
9 PD; 10 HC
NA
Yes
No
No
Neu
Discrimination
RT; ERP
Discrimination: PD
HC; RT: PD HC;
ERP: response in parietal cortex in PD/ in amygdala and
temporal cortex in HC (F)
(Continued )
Yes
No
Static faces: F, S,
No
TABLE 1. (Continued)
Disease
Authors
duration
Cognitive
Dopa
Control
assessment
Yes
Depression
No
Yes
Anxiety
task
No
Yes
Emotional stimuli
Sentences: A, D, F,
No
Yes
No
No
No
Sentences: H, Sa,
No
No
No
Sentences: H, Sa.,
Sentences: A, S,
Sa, cheerful
Dependent variables
Discrimination;
categorization
RFE; PFE; PEP
Discrimination: PD
No
HC; categorization PD < HC
Breitenstein
et al.22 (1998)
7 H&Y I/PD; 7
H&Y II/PD; 12 HC
44.0 6 28.9
months (I); 62.4
6 29.5 months
(II) (mean 6
SD)
Yes
Yes
No
No
Yes
Sentences: H, Sa.,
A, Neu
Discrimination;
categorization
RFE; intermodal
emotional task
Discrimination and
No
categorization: stage II PD < HC;
discrimination and categorization: stage I PD HC
Breitenstein
et al.40 (2001)
14 advanced
PD; 6 early
PD; 16 HC
59.1 6 58.3
months (adv.); 16.2 6 7.8
months (early) (mean 6 SD)
Yes
(mod.);
No (early)a
Yes
Yes
No
Yes
Congruent and
incongruent sentences: H, Sa, A, Neu
Categorization
Pitch variation
manipulation
Categorization: advanced
PD < HC (greater for incongruence);
categorization: early PD HC; categori- zation: early
advanced PD; pitch: PD HC
Sociodemo
graphic, cognitive, and clinical (ns)
Caekebeke
et al.23 (1991)
21 PD; 14 HC
5.5 6 NA years
(mean 6 SD)
Yes
Yes
No
No
No
NA
NA
speech; PEP; RFE
REP: PD HC;
No
production speech: PD HC
Clark et al.24 (2008)
20 PD; 23 HC
7.3 6 4.2 years
(mean 6 SD)
Yes
Yes
Yes
Yes
No
NA; A, D, F, H, Sa,
S
Categorization
RFE interpersonal
problem
Categorization: PD
HC
Depression anxiety (-)
(PD); depression anxiety (ns) (HC);
sociodemographic, clinical, cognitive (ns)
Dara et al.41 (2008)
16 PD; 17 HC
8.2 6 3.6 years
(mean 6 SD)
Yes
Yes
Yes
No
Yes
Pseudowords, sentences: A, D, F, Sa, Neu, H, S
Categorization (pseudowords and senten- ces); valence (analogical scale); in- tensity (analogical scale) (pseudowords only)
RFE/recognition of
emotions from verbal stimuli
Categorization of
sentences: PD
HC; categorization of pseudowords: PD < HC; valence: PD <
Production of
on
HC; intensity: PD
HC; verbal stimuli: PD HC
Clinical (ns)
Kan et al.29 (2002)
16 PD; 24 HC
NA
A, F, S, D
RFE/recognition of
emotions from verbal stimuli
Categorization: PD
HC
Sociodemographic,
clinical, cognitive (ns)
Yes
Yes
Yes
No
No
Sentences: H, Sa,
TABLE 1. (Continued)
Authors
Disease
duration
Cognitive
assessment
Control
task
11 PD; 11 HC
n
Dopa
Depression
Emotional stimuli
Anxiety
Dependent variables
Others
Results
Correlations
Lloyd42 (1999)
16 PD; 20 HC
NA
Yes
Yes
Yes
Neu
Discrimination;
categorization
Ling. Prosody discrimination and categorization
Discrimination: PD
No
HC; categorization: PD < HC; linguistic discrimination and
categorization: PD
HC
Mitchell and
Boucas43 (2009)
Sentences: H, Sa;
nouns: H, D, Sa, F
Categorization
No
PD HC
Disease duration (-),
motor (-)
33 PD; 33 HC
8.0 6 4.6 years
Yes (exc. Yes
No
No
Yes
(mean 6 SD)
3)
21 PD; 21 HC
3.9 6 1.9 years (mean 6 Yes (exc. Yes
Yes
No
Yes
SD)
1)
Pell and
Leonard44 (2003)
8.0 6 NA years
(mean 6 SD)
Pseudowords: H, A,
D, Sa, S
Yes
Yes
No
No
Yes
Sentences/pseudowords/filtered sentences (without seg- mental informa- tion): A, Sa, H
Discrimination;
categorization; intensity (Likert)
Discrimination; categorization
Linguistic prosody
discrimination; recognition of emotions from verbal stimuli; RFE
Stress
comprehension
Discrimination and
categorization: PD < HC; intensity: PD < HC (D, Sa)
Discrimination and categorization: PD < HC; stress: PD HC
Cognitive, control (ns)
(PD)
No
Schroder et al.40 (2006)
14 PD; 14 HC
4.8 6 5.5 years
(mean 6 SD)
Yes
Yes
Yes
No
No
First name: Sa,
Neu, H
Passive listening;
categorization
EEG (passive); RT
(categorization)
Categorization: PD <
No
HC; EEG: Decreased mismatch negativity for S in passive conditioning; RT:
Neu < emotions (PD and HC)
Scott et al.46 (1984)
28 PD; 28 HC
8.0 6 NA years
(mean 6 SD)
No
Yes
rimination
Speech production;
linguistic prosody
production; PEP
PD < HC for all tasks
No
Ve lez-Feijo
et al.47 (2008)
35 PD; 65 HC
6.9 6 4.2 years
(mean 6 SD)
Yes
Yes
Yes
No
No
H, Neu
Categorization
No
PD > HC
Yip et al.37
56 bilateral
7.2 6 4.0 years
Yes
Yes
No
No
No
Discrimination;
RFE
Discrimination and
Clinical (ns); visuospatial
(2003)
PD; 8 R
(bilateral PD)/
PD; 64 HC
2.8 6 1.6yrs (R
PD); (mean 6
SD)
Sentences: A, Sa,
Depression ()
Sentence: H, Sa, A,
S, D, F
Yes
No
Yes
No
No
No
Yes
No
No
Sentences: A, S,
Sa, cheerful
No
No
Sentences: H, S,
interest, Sa, F,
No
TABLE 1. (Continued)
Disease
Authors
9 PD; 10
duration
Cognitive
Dopa
NA (1980)
Caekebeke
et al.23 (1991)
with
somatic pathology
21 PD; 14 HC
5.5 6 NA years
(mean 6 SD)
unpleasant,
unusual)
Yes
Yes
No
No
Yes
Neu
Voluntary production;
spontaneous production; independent raters: yes
Speech production;
RFE; REP
Voluntary: PD < HC
No
(anger); spontaneous: PD < HC; speech:
PD HC
First name: Neu,
Sa, H
Voluntary production;
imitation; independent raters: no
Speech production
Production: PD < HC;
No
imitation: PD HC; speech: PD HC
Mo bes et al.49
16 PD; 16 HC
4.8 6 5.5 years
(2008)
(mean 6 SD)
NA
Control
assessment
Depression
Anxiety
task
Emotional stimuli
No
No
No
No
NA; A, hesitating,
Yes
Yes
Yes
No
Yes
9 PD; 10 con-
NA
(1980)
trol group
(patients with somatic pathology)
people, scenic,
unpleasant, unusual)
Spontaneous PFE;
independent raters: yes
PEP
Spontaneous PFE: PD <
No
HC
Jacobs et al.28 (1995)
11 PD; 17HC
NA
Yes
intensity); independent raters: yes
RFE
Intensity PFE: PD < HC;
posed PFE: PD <
HC for A and Sa
Perceptual and imagery
task ()
Katsikitis and
Pilowsky52 (1988)
Katsikitis and Pilowsky53 (1991)
8 PD; 9 HC
7.3 years
(SD:NA)
21 PD; 12 HC
6.32 6 4.75 years
(mean 6 SD)
Yes
No
Yes
Yes
(frequency and intensity); independent raters: no
Yes
No
Yes
No
(frequency and intensity); independent raters: yes
No
PD < HC for degree of
mouth opening and
frequency of smiling
No
Yes
No
Yes
No
No
Yes
No
No
Sentences: A, D, H,
Neu, Sa, S
NA
Sentences: H, S,
Yes
NA
Yes
Yes
NA
No
Yes
No
NA
Yes
No
Cartoons pictures
Spontaneous PFE
No
Cartoons pictures
Spontaneous PFE
NA
No
Relate emotional
experience
(pleasant or
unpleasant)
Pictures (familiar
No
Intensity : PD < HC;
frequency: PD < HC
Depression ()
Depression ()
Madeley et al.32 (1995)
9 PD; 9 HC
NA
Yes
static faces: Sa, A, D, Neu
Expressivity (posed and
mimicry) (Likert); independent raters: yes
RFE
Expressiveness: PD <
HC
(Continued )
No
Yes
Yes
Yes
Normal and PD
No
TABLE 1. (Continued)
Disease
No
No
Authors
duration
Pitcairn et al.54
(1990)
4 PD; 12 HC
NA
Cognitive
Dopa
NA
Control
assessment
Depression
Anxiety
task
Emotional stimuli
Dependent variables
No
Yes
Yes
No
Interview
Saku and
Ellgring55 (1992)
Simons et al.56
(2004)
24 PD; 24 HC
6.7 6 5.4 years
(mean 6 SD)
19 PD; 26 HC
54.8 6 42.28
months (means
6 SD)
Yes
No
No
No
No
Odors (pleasant,
unpleasant)
Yes
Yes
Yes
No
No
Video clips
(comics); social interaction
raters: ND
Spontaneous PFE; independent raters: yes
Spontaneous PFE; posed PFE; imitation PFE (Likert); independent raters: yes
PD < HC; posed
smiles: PD > HC;
frequency of smiling: PD HC
No
Spontaneous prod: PD
< HC (for unpleas- ant odors)
No
Spontaneous RFE: PD <
HC; intensity of posed PFE: PD < HC (except A)
No
Disease duration, social context, subjective
feeling ()
Simons et al.57 (2003)
22 PD; 22
patients with somatic pathology
6.82 6 3.57 years
(mean 6 SD)
Odors (pleasant,
unpleasant)
Spontaneous PFE; posed
PFE; imitation PFE; rated by FACS; independent raters: yes
No
Intensity: PD HC;
No
posed, spontaneous and imitation
frequency: MP < HC
Smith et al.58 (1996)
12 PD; 12 HC
6 years (median
duration)
Film excerpts: Sa,
H, F, A, D, Neu
Spontaneous PFE; posed
PFE; rated by FACS; independent raters: yes
No
Posed PFE: PD HC;
No
spontaneous PFE: PD
< HC
The table is divided into emotional subcomponents and shows, for each paper, the first author of the study, the publication year of study, the number of participants included in the study, the duration of th
disease, the presence or not of dopatherapy during the testing, the presence or not of a cognitive and mood evaluation, the presence or not of a control task (the control tasks are specific to each emotional
aNo a posteriori verification if de novo PD patients responded to dopa. A, anger; BOLD fMRI, blood oxygenation level-dependent functional magnetic resonance imagery; cog., cognitive; D, disgust;
Some authors have argued that the deficit in the pro- duction of facial and vocal emotional expressions explains the deficit in emotion recogn
Discussion
Synthesis
We have found a large body of evidence pointing to the existence of emotional disorders in PD. These con- cern several components of emot
Although the pathophysiological mechanisms sub- tending these emotional disorders in PD are still not fully understood, such disturbances
(2) impairment of the dopaminergic pathways and/or the BG in emotional processing.
The amygdalas involvement in emotional processing is now well documented in the literature.63 For this reason, presumed impairment of th
Apart from the amygdala dysfunction hypothesis, the most widely held hypothesis is that dopamine
the thalamus, putamen, and head of the caudate nucleus has been found in response to emotional prosody processing.101104 Recently, activity of the STN was also observed in response to voca
Compelling evidence that the BG are engaged in the processing of speech prosody has also been gathered from clinical sources. In a compara
109
The studies reporting emotional disturbance in PD cited herein point to the involvement of the BG in emotional processing, which has also b
Using fMRI, several studies have reported subcorti- cal activation during emotional processing. Activity of
These data fit in well with observations that emotional processing is typically impaired in patients with BG degeneration due to Huntingtons disease, 97,112 reinforcing the view that the BG pl
Thus, there is growing evidence in favor of the involvement of the BG in emotional processing, not only directly, but also through their conn
Conclusion
The present review provides a synopsis of the emo- tional disturbances observed in PD. The disruption of several components of emotional p
Acknowledgments: We thank Prof. David Sander and Dr. Sebas-
tian Korb (Swiss Center for Affective Sciences, University of Geneva, Switzerland) for their advice on theoretical matters, as well as Elizabeth Wiles-Portier for preparing the m
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mesolimbic dopamine system that modulates their func- tion, are thought to be involved in emotional processing. As Parkinsons disease is histopathologically character- ize
cortical and mesolimbic circuits, ending with the conclu- sion that both these pathways are indeed involved in emotional processing. VC 2011 Movement Disorder Society
arousal, motor expression, subjective feeling and, according to some researchers, action tendencies and cognitive processes as well) in response to environ
ssociated with emotional states. 6 The concept of
he concept of subjective feeling refers to the fact that, in humans, emotions are associated with an internal subjective state. 8
partic- ular its episodic nature 911 and the idea that emotions are normally generated by events that have important meaning for the organism. In turn, these
roc- essing. Even if PD involves multiple neuronal sys- tems, 12 PD is histopathologically characterized by selective, progressive, and chronic degeneration
eview is divided into 2 sections. In the first section, we focus on information pertaining to emotional processing in PD. In the second section, we discuss th
emotional processing and PD. The databases were selected using PubMed services with the following keywords: Parkinsons disease, emotion, facial expr
hese include not only changes in the emotional experience associating subjective feeling with physiological arousal, but also the impaired production and
soci- ated with physiological measures. Participants are shown stimuli with a positive, negative, or neutral va- lence (eg, pictures from the International Af
e the highest level of physiological arousal, which the authors ascribed to emotional blunting in PD. No dif- ference, however, was found between the 2 gr
sults showed that the startle reflex was selectively blunted in PD patients compared with HC in the aversive stimulus condition. This reflex was intact, how
y to fear-eliciting stimuli as opposed to other types of aver- sive pictures was investigated by Miller et al. 15 Results did not support the hypothesis of a spec
ogi- cal arousal emotional components in PD. These have been linked to the difficulty encountered by PD patients in assessing their feelings on the basis
processing in PD
ictures:
(Likert)
D
Dependent variables
Others
Results
Correlations
ional words:
Arousal (Likert); valence
No
Arousal and valence: PD
No
(Likert)
< HC
ctures:
Arousal (Likert); Valence
Startle eye blink
Arousal and valence PD
Sociodemographic,
(Likert)
< HC (Neg); startle
clinical, and
Categorization; matching
REP
Categorization; matching
PEP; REP
Discrimination;
neuropsychological
variables (ns)
Dependent variables
Others
Results
Correlations
Discrimination
No
Discrimination early PD
Cognitive, visuospatial,
HC; advanced PD
categorization
Dependent variables
Categorization
No
categorization:
bilateral PD < HC;
discrimination: right
PD HD;
categorization right
PD < HC
Others
PEP
Results
()
Correlations
categorization
Voluntary production
(accuracy); i
ndependent raters:
yes
categorization:
bilateral PD < HC;
discrimination: R PD
HC; categoriza- tion: R PD < HC
()
REP
Production: PD (intact
and impaired mixed)
(); Others clinical,
< HC; production:
impaired PD < HC;
production: intact PD
Dependent variables
Others
PFE
Results
Correlations
No HC
Dependent variables
Others
Gestures and
posture
Results
Expressiveness: PD <
HC; happy smiles:
Correlations
No
ed by the human voice (ie, emotional prosody) in PD, 2022,29,37,3942,44,46,61 studies of emotional facial expression (EFE) recognition have yielded some pa
abilities in PD in order to disentangle apparent discrepancies in results, notably for the facial modality. The authors identified 7 potential moderators. T
s of prosodic recognition may yield more variance in attempts to detect group differences. As far as task type is concerned, results reported by Gray and
ed ei- ther to the level of motor disability or to depression status, suggesting that motor disability (and/or depression) and the deficit in emotion recog
ent- related potential study, diminished amygdala activity in response to the perception of fearful facial expres- sions was observed in medicated PD patie
d vocal expressions, which we believe could be partially explained by amygdala dysfunction. It also strongly suggested that discrepancies in results were d
to akinesia, rigidity, and increased reaction times of facial muscles. As the disease progresses, the face becomes frozen and inexpressive. Amimia can ha
esized that voluntary emotional movements are less affected than spontaneous activity. This hypothesis was vali- dated in the study by Smith et al., 58 wh
rep- ancy in results for the emotional production modality. The first set of factors concerns aspects of the emotion production tasks used by researchers (sti
e sub- ject of a number of studies. 20,21,39,49,50 Its interpreta- tion is still a matter of considerable debate, with some researchers arguing that it should be reg
s explains the deficit in emotion recognition processes in PD. Their hypothesis is based on the simulation theory, whereby, through a process of facial
part, experience deficits in emotion recognition because they have a reduced ability to spontaneously mimic displays of emotion.
e con- cern several components of emotion, including subjec- tive feeling, physiological arousal, and motor expression, and several input modalities, name
not fully understood, such disturbances may well arise from (1) disruption of amygdala function in PD and
this reason, presumed impairment of the amygdala in PD has been put forward as an explanation for the emo- tional disorders observed in this pathology3
nifi reduction in the neuron density of the basolateral nu- cleus, with the most massive loss (approximately 30%) occurring in the cortical nucleus. This fi
sults demonstrating the functional role of the BG in emo- tional processing in nigrostriatal lesion patients have
d suggest that dopaminergic neurons facilitate the selection of the most appropriate strategy for a given situation. 79
- nists and antagonists. For example, a study by Law- rence et al. 80 demonstrated that EFE recognition for anger was diminished following the administrati
otably clinical studies of patients with neurological patholo- gies resulting in disturbed dopaminergic systems. Emo- tional disorders have been reported no
emotional processing, which has also been docu- mented in patient, lesion, and fMRI studies. 100103
7,112 reinforcing
the view that the BG play an essential part in systems devoted to emotional processes.
only directly, but also through their connections with brain structures known to be involved in emotional processing.
n of several components of emotional processing does indeed point to the functional involvement of the do- paminergic pathways and BG in these process
pas- sions. In: Strongman KT, ed. International review of studies on emotion. New York: Wiley & Sons Ltd; 1991: 187225.
2008; 29:219227.
sease or chronic progressive multiple sclerosis. Bull Psychonom Soc 1989;27:361364.
9;37: 11551163.
Nat Neurosci 2005;8:145146.
motional prosody in meaningless speech. Neuroimage 2008;42: 919927.
vent- related functional MR investigation. Brain Lang 2003;86(3): 366376.
sody. Cereb Cortex (in press). (DOI:10.1093/cercor/bhr184)
stopathologically character- ized by the selective, progressive, and chronic degenera- tion of the nigrostriatal and mesocorticolimbic dopamine systems, it can therefore ser
well) in response to environ- mental events of major significance to the organism. These events may be either internal (eg, thoughts, sen- sations, memori
the organism. In turn, these 2 features underline the 2 main differences between affective states (such as mood) and emotions, namely: (1) dura- tion (ie,
ve, and chronic degeneration of the nigrostriatal and mesocorticolimbic dopamine systems, and offers an opportunity to study the possible influ- ence of th
econd section, we discuss the functional role of the striato-thalamo-cortical circuits in emo- tional processing.
disease, emotion, facial expres- sion, emotional prosody, subjective feeling, arousal. Studies dealing with the emotional effects of subthala- mic nucleus de
he impaired production and recogni- tion of emotions conveyed by faces or voices. The results of these studies are summarized in Table 1. 1358
res from the International Affective Pic- ture System 13,15,16 or words with emotional connotations14) and are then asked to self-report va- lence and physiol
, was found between the 2 groups of participants with respect to electroencephalography response patterns. These 2 sets of results were inter- preted as hig
n. This reflex was intact, however, in the positive- and neutral-valence conditions. To account for their results, the authors hypothesized that PD makes it h
port the hypothesis of a specific deficit in emotional reactivity to fearful pictures, as PD patients also showed reduced reactivity to mutilation pictures, rela
ng their feelings on the basis of their physical and physiological sensations. Some authors, for instance, have claimed that PD patients suffer from alexithy
osia, for the recognition of emotional prosody we considered an audiometric screening procedure, for the production of emotional prosody we considered an evaluation of speech production, and for subjective feeling it dep
FACS, facial action coding system; F, fear; H, happiness; H&Y, Hoehn & Yahr; HC, healthy controls; IQ, intelligence quotient; L, left; Likert, Likert scale; ling., linguistic; mod., moderate (stage of PD); NA, not available;
nition have yielded some partic- ularly ambivalent results. Whereas some authors have reported diminished EFE recognition in Parkinsonian individuals
ed 7 potential moderators. Three of these con- cerned aspects of the emotion recognition tasks used by researchers (stimulus modality, task type, and emo
results reported by Gray and Tikle-Degnen 62 indicate that both facial expression and prosody identification and discrimination tasks bring to light greater
d the deficit in emotion recogni- tion stem from different forms of brain pathology. As far as executive functions and visuospatial deficits are concerned
served in medicated PD patients com- pared with HC. 38
screpancies in results were due to the heterogeneous clinical profiles of the PD patients included in these studies, illustrated in Table 1.
study by Smith et al., 58 which showed that although PD patient and HC groups assessed the emotional intensity of video clips in the same way, the PD p
asks used by researchers (stimulus modal- ity, task type, and emotion displayed). The second set of factors concerns the characteristics of the PD patient
arguing that it should be regarded as a purely motor, articulatory disorder,70 and others sug- gesting instead that it is an emotional defi- cit.23,28,39,48,50,58 Th
through a process of facial feed- back, facial muscular activity can modulate emo-
veral input modalities, namely emo- tional prosody, facial expressions, and verbal labels (ie, words with emotional connotations), and may be present fro
observed in this pathology36,38 and has been the focus of a number of studies7275 (cf. infra). Neuropathological research findings support
n of vocal expressions of emotions are far more prevalent in patients with focal lesions that affect the BG than in ones with other lesion sites. 106108
ed following the administration of a dopaminergic antagonist. Similarly, an fMRI study revealed that the activity of several limbic regions (amygdala, hipp
orders have been reported not only in PD, but also in schizophrenia (for a review, see Edwards et al. 85), autism,8693 attention-deficit hyperactivity disord
ways and BG in these processes. This review also underlines the need to control for poten- tial confounding factors linked to the emotional tasks but also to
opamine systems, it can therefore serve as a model for assessing the functional role of these circuits in humans. In the pres-
g, thoughts, sen- sations, memories) or external (eg, other peoples behavior, a change of situation, an encounter with a novel stimulus). 15 The concept of
otions, namely: (1) dura- tion (ie, mood lasts longer than emotion) and (2) the presence or absence of an external/internal event (ie, mood does not necessa
udy the possible influ- ence of these dopaminergic pathways on emotional processing.
ffects of subthala- mic nucleus deep brain stimulation (STN DBS) were excluded from the present review, as we believe that they tell us more about the S
f results were inter- preted as highlighting a dissociation between the early automatic processing of emotional information and the subsequent processes o
hypothesized that PD makes it harder for patients to gauge the threaten- ing value of negative stimuli, possibly due to reduced activation of the amygda
ctivity to mutilation pictures, relative to other types of negative pictures. Further analyses revealed that startle eye-blink magnitude (measured while partic
PD patients suffer from alexithymia. 59 Alexithymia is defined as the inability to identify and describe ones feelings, and to distinguish between feelings a
ech production, and for subjective feeling it depends on the stimuli, when stimuli are visual we considered an evaluation of visuospatial and agnosia evaluation). The table shows also the emotional stimuli and the emotions
od., moderate (stage of PD); NA, not available; ND, no data; Neg, negative; Neu, neutral; off, off dopa condition; on, on dopa condition; Pos, positive; PD, Parkinsons disease; PEP, production of emotional prosody; PET,
ion in Parkinsonian individuals compared with HC, 24,26,2830,3437,39 others have failed to demonstrate any difference at all between the two.17,22,25,32
ulus modality, task type, and emo- tion displayed). The other 4 concerned the PD patients themselves (motor disability, depression status, per- formance on
nation tasks bring to light greater deficits than rating tasks, though with contrasting patterns for facial expressions and prosody. Discrimination tasks revea
uospatial deficits are concerned, results showed that (1) the facial emo- tion recognition deficit in PD goes beyond a general deficit in face processing, an
ed in Table 1.
o clips in the same way, the PD patients displayed reduced expressiveness when watching these extracts. In the condition where facial expressions were pr
haracteristics of the PD patients themselves, including medication status, depression status, 68,69 and cognitive deterioration (eg, dysexecutive syndrome)
motional defi- cit.23,28,39,48,50,58 This question was addressed by Mo bes et al.,49 who found that although PD and HC did not differ in a nonemotional m
otations), and may be present from disease onset. As far as the recognition of emotions in PD is concerned, the deficit appears to be cross-modal, in that it
h findings support
ones with other lesion sites. 106108 In a recent lesion study featuring a
al limbic regions (amygdala, hippocampus, anterior cingulate cortex) during the perception of unpleasant images was reduced in HC who had been given a
ention-deficit hyperactivity disorder,9496 and Huntingtons disease.9799
to the emotional tasks but also to the sociodemographic and clinical charac- teristics of the PD patients themselves. From a clinical point of view, the cons
ovel stimulus). 15 The concept of physiological arousal refers to the fact that different types of physi-
that they tell us more about the STNs functional role in emotional processing in general than about the speci- ficity of this processing in PD. We also hand
n and the subsequent processes of appraisal. A subsequent study by Hillier et al. 14 supported this interpretation, in that the PD patients self-reports of
magnitude (measured while participants were viewing emotional stimuli) varied with arousal level in the HC, but not in the PD group. The authors sugges
to distinguish between feelings and bodily sensations of emotional arousal. 60
ws also the emotional stimuli and the emotions presented to the participants, the dependent variables, the potential assessment of others behavioral but also nonbehavioral measures, a summary of the results reported in the
se; PEP, production of emotional prosody; PET, positron emission tomography; prod., production; PFE, production of facial expression; R, right; REP, recognition of emotional prosody; RFE, recognition of facial
epression status, per- formance on executive function and visuospatial abil- ity tasks, and medication status). First of all, they found a robust link between
sody. Discrimination tasks reveal a significantly greater deficit in facial emotion recognition, and iden- tification tasks a significantly greater deficit in pro
eral deficit in face processing, and (2) there is a link between prosodic emotion recognition and working memory, suggesting that deficits in prosodic emo
where facial expressions were produced on command (voluntary), there was no difference between the 2 groups. By con- trast, other studies have reported
tion (eg, dysexecutive syndrome) owing to the spread of the lesions to nondopaminergic pathways.12 The problem is that studies exploring the productio
id not differ in a nonemotional motor prosodic con- dition, PD patients exhibited a significant reduction in the production of emotional prosody. The autho
pears to be cross-modal, in that it is manifests itself in the rec- ognition of emotion from both faces and voices. How- ever, it seems to be greater for the re
uced in HC who had been given a dopaminergic antago- nist. 81 These results have been confirmed by other fMRI studies using dopamine manipulations. 82
m a clinical point of view, the consequences of these emotional disturbances in daily living and their relationship to mood and behavioral disorders such as
s processing in PD. We also hand searched all the relevant journals. In addition, we examined the bibliographies of key articles to glean further publica- tio
t the PD patients self-reports of physiological arousal and concomitant assessments of emotion were blunted, compared with those of the HC group using
he PD group. The authors suggested that decreased aversion-modulated startle might be driven by reduced reactivity to highly arousing negative stimuli, r
sures, a summary of the results reported in the study, and the correlations between emotional results and secondary variables.
emotional prosody; RFE, recognition of facial expression; RT, reaction time; S, surprise; Sa, sadness; SD, standard deviation.
hey found a robust link between PD and impaired recogni- tion of emotion from faces and voices confirming the existing literature and indicating that the
ignificantly greater deficit in proso- dic emotion recognition. As far as the emotion displayed factor is concerned, Gray and Tickle-Deg- nen 62 also obse
ting that deficits in prosodic emotion recognition in PD stem partially from working mem- ory constraints. Finally, as far as medication status is concern
- trast, other studies have reported a deficit in voluntary EFE production alone, 21,28,67 or in both spontaneous EFE and voluntary EFE production in PD
at studies exploring the production of facial expressions vary considerably in their emotional meth- odology, as well as in the availability of clinical data (T
n of emotional prosody. The authors concluded that dysprosody in PD cannot be ascribed solely to an articulatory impairment.
r, it seems to be greater for the recognition of emotion from prosody than for the recognition of emotion from facial expressions. Furthermore, PD patients
and behavioral disorders such as depression, anxiety and apathy, often observed in PD, remain to be clarified.
rticles to glean further publica- tions. Our search was restricted to English-language papers and spanned the period from January 1990 to January 2010. Fo
ghly arousing negative stimuli, rather than to a specific category (ie, fear or disgust) of emo- tional stimuli.
literature and indicating that the deficit in emotion recognition in PD is cross-modal (stimulus modality factor). That said, the deficit appeared to be
y and Tickle-Deg- nen 62 also observed that individuals with PD were more impaired in the recognition of negative emotions (anger, disgust, fear, and sadne
as medication status is concerned, although the authors noted a larger impairment effect size among patients who were in a hypodopaminergic state at t
ssions. Furthermore, PD patients are more impaired in the recognition of nega- tive emotions (anger, disgust, fear, and sadness) than in the recognition of
anuary 1990 to January 2010. Forty-three articles were identified as being relevant to the question of emotional processing in PD. No English-language pa
aid, the deficit appeared to be greater for the recognition of emotion from pros- ody than from facial expressions. The authors sug- gested 3 potential ex
ns (anger, disgust, fear, and sadness) than in that of rela- tively positive emotions (happiness, surprise). Accord- ing to the authors, these results were not s
in a hypodopaminergic state at the time of testing, they failed to find a significant difference in effect sizes between on and off dopa conditions. It should
pact of cogni- tive impairment or dopamine repletion. Accordingly, even though several hypotheses can be put forward, it is difficult to compare these diff
dness) than in the recognition of relatively positive emotions (hap- piness, surprise). Apparent discrepancies in results could be attributed to several confo
g in PD. No English-language papers exploring emo- tional processing in PD patients without DBS were excluded from the present review.
authors sug- gested 3 potential explanations for this finding. First, emotional prosody recognition may be more suscepti- ble to the reduction in working m
e authors, these results were not simply artifacts reflecting different levels of difficulty across
nd off dopa conditions. It should be noted that this meta-analysis only investigated behav- ioral results, and did not touch on physiological results, as me
t is difficult to compare these different studies in order to identify the root causes of their apparently discrep- ant results.
ould be attributed to several confounding factors. The first set of factors concerns aspects of the emo- tional task (eg, instructions, stimulus modality, task
he present review.
ble to the reduction in working memory capacity that is often noted in PD. Second, the BG may play a more
h on physiological results, as measured by functional magnetic resonance imaging (fMRI), for example. In an fMRI investiga- tion of PD patients perfor
ructions, stimulus modality, task type, and emotion displayed), whereas the second set of factors concerns characteristics of the PD patients themselves (m
estiga- tion of PD patients performing a task in which they had to match faces expressing anger or fear, patients were assessed both on and off dopaminer
of the PD patients themselves (medication status, depression status, and performance on cognitive and visuospatial ability tasks). The problem is that thes
sessed both on and off dopaminergic medica- tion. No behavioral difference in terms of EFE recog- nition abilities was found either between the on and
y tasks). The problem is that these studies, especially research on the production of emotions, vary so widely in the emotional methodology used by res
und either between the on and off dopa conditions or between PD patients and HC. However, reduced amygdala activation was observed in patients
motional methodology used by researchers, as well as in the clinical profile of the PD patients, that comparisons are well nigh impossible (Table 1).