REVIEW

Emotional Processing in Parkinsons Disease: A Systematic Review

Julie Pe ron, PhD,1-3* Thibaut Dondaine, MSc,1,2 Florence Le Jeune, MD, PhD, 1,4 Didier Grandjean, PhD,3 and Marc Ve rin, MD, PhD1,2

(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

ABSTRACT: Parkinsons disease provides a useful

model for studying the neural substrates of emotional processing. The striato-thalamo-cortical circuits, like the mesolimbic dopamine system that modulates

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

Most emotion theoreticians agree that emotions are

episodes of synchronized changes in several of the organisms components (including physiological arousal, motor expression, subjective fe
ological activation (autonomic nervous system, hor- mone levels, and certain neurotransmitters) are associated with emotional states. 6 The

-----------------------------------------------------------*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.

motor expression refers to the fact that emotional

episodes induce changes not just in facial expressions and speech, but also in gestures and posture.7 The concept of subjective feeling refe
This last definition encompasses several features that are deemed to be inseparable from emotion, in partic- ular its episodic nature 911 and th
Parkinsons disease (PD) constitutes a useful model for studying the neural substrates of emotional proc- essing. Even if PD involves multip
Taking into account the limitations of this model, we seek in the present review to provide a synopsis of
186

Movement Disorders, Vol. 27, No. 2, 2012

EMOTION

A ND

PD

the emotional disturbances observed in PD, in order

to underline the functional roles of the dopaminergic pathways and basal ganglia (BG). The present review is divided into 2 sections. In the f

ew: Search Strategy and Selection Criteria

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

ctive Feeling and Physiological Arousal

Emotional experience in PD has been investigated using emotional induction procedures generally associ- ated with physiological measures.
Wieser et al.16 also carried out electroencephalogra- phy recordings during the rapid presentation of emo-

tionally charged pictures. PD patients reported a lower

level of physiological arousal than healthy controls (HC) for those items judged by the latter to induce the highest level of physiological arou
In Bowers et al.,13 a sudden noise was used to trig-

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

Subjective feeling and arousal in Parkinsons disease

Bowers et al.13
(2006)

23 PD; 17 HC

9.9 6 5.9 years

(mean 6 SD)

Yes

Yes

Yes

No

Hillier et al.14

8 PD; 15 HC

514 years (range)

Yes

No

No

No

(2007)
Miller et al.15
(2009)

24 PD; 24 HC

5.5 6 3.6 years

(mean 6 SD)

Yes

Yes

Yes

No

Wieser et al.16 (2006)

14 PD; 14 HC
6.9 6 4.5 years
(mean 6 SD)
Yes
No
No
No
No
Neg, Pos, Neu
Arousal (Likert); valence
(Likert)
EEG
Arousal: PD < HC;
No
Valence: PD HC; EEG: PD HC
Recognition of facial expressions in Parkinsons disease
Adolphs et al.17 (1998)
18 PD; 13 HC
7.8 6 4.0 years
(mean 6 SD)
Yes
Yes
Yes
No
Yes
F, H, Neu, Sa, S
Categorization; intensity
(Likert)
No
Categorization and
intensity: PD HC
Categorization and matching: PD < HC (F and Sa)
IQ, prosopagnosia,
depression, gender (ns)/age (-)/
education ()
Depression executive
functions, nonverbal IQ, motor and duration (ns)
Ariatti et al.18
27 PD; 68 HC
113 years (range)

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/

8.2 6 5.3 years

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

Static faces: H, Sa,

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

Recognition of emotional prosody in Parkinsons disease

Ariatti et al.18 (2008)
11 PD; 68 HC
NA
Yes
Yes
H, Sa
Discrimination;
categorization
RFE; linguistic
prosody dis- crimination and categorization
Discrimination and
categorization: PD <
HC all tasks
Categorization: PD (intact and impaired
Depression, executive
functions, nonverbal IQ, motor, duration (ns)
Clinical and sociodemographic
Benke et al.39
22 cog. intact
9.8 6 6.0 years
Yes
(1998)
PD; 26
(intact); 9.9 6
cog.
impaired
PD; 18 HC
4.5 years
(impaired) (mean 6 SD)
mixed) HC; categorization: impaired PD < HC; categori- zation: intact PD HC
(ns)
Blonder et al.20 (1989)
21 PD; 17 HC
NA
Yes
No
puzzled, A
Linguistic prosody
discrimination; syntactical com- prehension; stress compre- hension; PEP;
RFE
Categorization: PD <
No
HC; linguistic dis- crimination PD HC; syntactical: PD
HC; Stress: PD <
HC
Borod et al.21 (1990)
20 PD; 21 HC
NA
Yes
No
A, Neu

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

First name: H, Sa,

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

Production of emotional prosody in Parkinsons disease

Benke et al.39
22 cog. intact
9.8 6 6.0 years
Yes
(1998)
PD; 26
(intact); 9.9 6
cog.
4.5 years
impaired
(impaired)
PD/18 HC
(mean 6 SD)
Blonder et al.20 (1989)
21 PD; 17 HC
NA
Yes
No
A
Spontaneous prod.
(accuracy and intensity); imitation (accuracy); independent raters: yes
Linguistic prosody
production and repetition
HC
Spontaneous production No and repetition: PD <
HC; linguistic production PD < HC; linguistic repetition:
PD HC
Borod et al.21
20 PD; 21 HC
NA
Yes
(1990)
D, Neu
Voluntary prod. (accuracy, intensity); inde- pendent raters: yes
RFE; PFE; REP
PD < HC
(Continued )

Yes

No

Yes

No

No

No

Yes

No

No

Sentences: A, S,
Sa, cheerful

NA: H, Sa, puzzled,

No

No

Sentences: H, S,
interest, Sa, F,

No

TABLE 1. (Continued)
Disease
Authors

Buck and Duffy48

patients

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

Pictures (familiar people,

scenic,

NA; A, hesitating,

Yes

Yes

Yes

No

Yes

Production of facial expressions in Parkinsons disease

Voluntary production
(accuracy, intensity); independent raters: yes
Voluntary production; independent raters: NA
Speech production;
aphasia
Speech prod./ ling. Prosody prod./ REP
Accuracy: PD < HC (A,
D); intensity: PD <
HC
REP: PD < HC; speech: PD HC; linguistic prosody: PD < HC
Sociodemographic,
clinical, cognitive (ns)
No
Pell et al.50
21 PD; 12 HC
3.9 6 1.9 years
Yes (exc.
Yes
(2006)
(mean 6 SD)
1)
Scott et al.46
28 PD; 28 HC
8.0 6 NA years
Yes
No
(1984)
(mean 6 SD)
Borod et al.21 (1990)
20 PD; 21 HC
NA
NA
No
No
interest, Sa, F, D, Neu
Posed PFE; independent
raters: yes
RFE/PFE/REP
Posed PFE: PD < HC
No
Bowers et al.13 2006
12 PD; 12 HC
5.5 6 2.5 years
(mean 6 SD)
Yes
Yes
Yes
No
No
No
A, and S); interraters agreement: no (automatic method)
No
Frequency and speed
No
PFE: MP < HC
Spontaneous PFE
(intensity, Pos and Neg valence); independent raters: yes
Social and
interpersonal functioning
Intensity PFE: PD < HC;
Pos emotions PFE:
PD < HC; Neg
emotions PFE: PD >
HC
Social functioning ()
Brozgold et al.51
20 PD; 21 HC
NA
NA
NA
(1998)
Buck and Duffy48

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,

Posed PFE (H, D, F, Sa,

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

Posed PFE (type and

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

Spontaneous and posed PFE;

independent

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;

Recognition of Facial Expressions

and Emotional Prosody
Whereas researchers have fairly consistently reported a deficit in the recognition of emotion conveyed by the human voice (ie, emotional p

The main aim of Gray and Tickle-Degnens62 recent

meta-analysis was to examine the influence of several potential moderators of emotion recognition abilities in PD in order to disentangle
substantial role in prosodic emotion recognition.44,63
Third, it is typically more difficult to infer emotion from prosody than from faces,64 meaning that tests of prosodic recognition may yield mo
emotions. Regarding clinical factors, results first
showed that, across studies, the level of emotion rec- ognition impairment did not appear to be related ei- ther to the level of motor disabi
with HC. This lack of response was partially restored by dopamine repletion.36 Additionally, in an event- related potential study, diminished
All in all, these results confirmed that PD is character- ized by a deficit in the recognition of facial and vocal expressions, which we believe c
Production of Facial Expressions and Emotional Prosody
A familiar symptom of PD, facial amimia refers to the impaired production of facial expressions due to akinesia, rigidity, and increased react
Researchers have long been interested in the possible distinction between voluntary and spontaneous facial
movements, insofar as they are subtended by 2 different neural networks: the pyramidal tract and the BG network.66 In PD, researchers have long hypothesized that voluntary emotional movem
As with the emotion recognition processes, several confounding factors can explain the apparent discrep- ancy in results for the emotional pr
Like amimia, dysprosody is a symptom of PD that is frequently reported by clinicians and has been the sub- ject of a number of studies. 20,21,3

Some authors have argued that the deficit in the pro- duction of facial and vocal emotional expressions explains the deficit in emotion recogn

tional experiences elicited by some external stimulus

(ie, something other than ones own facial actions).71 Therefore, individuals with PD may, at least in part, experience deficits in emotion reco

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.

sruption of Amygdala Function in PD

The amygdalas involvement in emotional processing is now well documented in the literature.63 For this reason, presumed impairment of th

the theory of amygdala impairment in PD. For example,

Harding et al.73 carried out postmortem examinations of nondemented PD patients and reported a signifi reduction in the neuron density of th

nergic Pathways and Emotional Processing

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

depletion of the mesolimbic pathway brings about a

dichotic listening paradigm, Grandjean et al.
demdysfunction of the limbic loop linking the BG to the
orbitofrontal cortex.76,77
There is a large body of evidence pointing to the involvement of dopamine in emotional processes (for a review, see Salgado-Pineda et al. 78).
onstrated the involvement of the caudate nucleus in
the processes that enable vocally expressed emotion to reduce spatial extinction syndrome. Similar results demonstrating the functional role o
110

From a neuroanatomical point of view, most of the

regions targeted by the projection of dopaminergic

been found not just in the vocal modality

facial one, too.111
but in the
neurons, especially those in the mesolimbic and mesocortical pathways, are known to play a role in the var- ious emotional processes.
Data from animal experiments also highlight the involvement of dopamine in emotional processes and suggest that dopaminergic neurons fac
The role of dopamine in emotional processes in humans can be tested by manipulating dopamine ago- nists and antagonists. For example, a s
Data suggesting dopamine involvement in emotional processes have come from other sources, too, notably clinical studies of patients with n

Ganglia (and Cortico-subcortical Loops)

and Emotional Processing

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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Marc Ve rin, MD, PhD1,2

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

in the online version of this article.

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

Arousal (Likert); valence

EMG; startle eye
Arousal: PD < HC
response
(Neg); valence: PD
(ns)

Correlations

Severity (); depression

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

eye blink did not

vary by arousal level
(PD) as is the case
in HC

Categorization; matching

REP

Categorization; matching

PEP; REP

Discrimination;

REP; PEP; PFE

neuropsychological
variables (ns)

Dependent variables

Others

Results

Correlations

Discrimination

No

Discrimination early PD

Cognitive, visuospatial,

HC; advanced PD

clinical (ns) (PD)

RT; BOLD fMRI

Matching: on PD < HC;

off PD < HC; bilateral amygdala response
absent in

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

Spontaneous PEP; independent raters: yes

PFE

Results

Education, speed index

cognitive and
sociodemographic
(ns)

Correlations

Spontaneous PEP: PD <

No HC

Dependent variables

Others

Spontaneous and posed PFE;

independent

Gestures and
posture

Results

Expressiveness: PD <
HC; happy smiles:

Correlations

No

er of participants included in the study, the duration of the

trol task (the control tasks are specific to each emotional components and stimuli: for the recognition of facial expression, we considered as a control task an evaluation of prosopagnosia, for the recognition of emotional pro
agnetic resonance imagery; cog., cognitive; D, disgust; early, early stage of PD; EEG, electroencephalography; EMG, electromyography; ERP, event related potential; exc., except; FACS, facial action coding system; F, fe

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

N was also observed in response to vocal emotions.105

ered from clinical sources. In a comparative lesion study, Cancelliere and Kertesz 106 concluded that deficits in the recognition of vocal expressions of em

r a review, see Salgado-Pineda et al. 78).

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

well as Elizabeth Wiles-Portier for preparing the manuscript.

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stopathologically character- ized by the selective, progressive, and chronic degenera- tion of the nigrostriatal and mesocorticolimbic dopamine systems, it can therefore ser

1 Movement Disorder Society

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.

inexpressive. Amimia can have a negative impact on PD patients interpersonal relationships. 65

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

the cortical nucleus. This fi

has since been confirmed in other investigations. 7275

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

arized in Table 1. 1358

self-report va- lence and physiological arousal.

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-

event (ie, mood does not necessarily have to have a trigger).

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

duced activation of the amygdala, a structure involved in

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

at all between the two.17,22,25,32,33

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

using dopamine manipulations.8284

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

with those of the HC group using emotional words.

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

oluntary EFE production in PD patients.56,57

the availability of clinical data (Table 1). For example, none of the studies of EFE production in PD controlled for the impact of cogni- tive impairment or

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).

ation was observed in patients in a hypodopaminergic state compared

igh impossible (Table 1).