(2012,Peron)Emotional processing in Parkinson's disease-a systematic review.xlsx

R E V I E W

Emotional Processing in Parkinson’s Disease: A Systematic ReviewJulie 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

Behavior and Basal Ganglia Research Unit (EM 425), University of Rennes 1, Hoˆ pital Pontchaillou, CHU de Rennes, Rennes, France

Neurology Unit, Hoˆ pital Pontchaillou, CHU de Rennes, Rennes, France

Neuroscience of Emotion and Affective Dynamics Laboratory, Department of Psychology and Swiss Center for Affective Sciences, University of Geneva, Geneva, Switzerland

Nuclear Medicine Department, Euge` ne Marquis AntiCancer Centre, Rennes, France

ABSTRACT: Parkinson’s 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 their function, are thought to be involved in emotional processing. As Parkinson’s disease is histopathologically characterized by the selective, progressive, and chronic degeneration of the nigrostriatal and mesocorticolimbic dopamine systems, it can therefore serve as a model for assessing the functional role of these circuits in humans. In the pres-

ent review, we begin by providing a synopsis of the emo-tional disturbances observed in Parkinson’s disease. We then discuss the functional roles of the striato-thalamo- cortical and mesolimbic circuits, ending with the conclu- sion that both these pathways are indeed involved in emotional processing. VC 2011 Movement Disorder Society

Key Words: amygdala; basal ganglia; emotion; Par- kinson’s disease

Most emotion theoreticians agree that emotions areepisodes of synchronized changes in several of the organism’s components (including physiological arousal, motor expression, subjective feeling and, according to some researchers, action tendencies and cognitive processes as well) in response to environ- mental events of major significance to the organism. These events may be either internal (eg, thoughts, sensations, memories) or external (eg, other people’s behavior, a change of situation, an encounter with a novel stimulus).1–5 The concept of ‘‘physiological arousal’’ refers to the fact that different types of physi-

ological activation (autonomic nervous system, hor- mone levels, and certain neurotransmitters) are associated with emotional states.6 The concept of

------------------------------------------------------------*Correspondence to: Dr. Julie Pe´ ron, CISA, 7 rue des Battoirs, 1205

Gene` ve, Suisse; [email protected]

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 emotionalepisodes induce changes not just in facial expressions and speech, but also in gestures and posture.7 The concept of ‘‘subjective feeling’’ refers to the fact that, in humans, emotions are associated with an internal subjective state.8

This last definition encompasses several features that are deemed to be inseparable from emotion, in partic- ular its episodic nature9–11 and the idea that emotions are normally generated by events that have important meaning for the organism. In turn, these 2 features underline the 2 main differences between affective states (such as mood) and emotions, namely: (1) duration (ie, mood lasts longer than emotion) and (2) the presence or absence of an external/internal event (ie, mood does not necessarily have to have a trigger).

Parkinson’s disease (PD) constitutes a useful model for studying the neural substrates of emotional processing. Even if PD involves multiple neuronal systems,12 PD is histopathologically characterized by selective, progressive, and chronic degeneration of the nigrostriatal and mesocorticolimbic dopamine systems, and offers an opportunity to study the possible influence of these dopaminergic pathways on emotional processing.

Taking into account the limitations of this model, we seek in the present review to provide a synopsis of186 Movement Disorders, Vol. 27, No. 2, 2012

E M O T I O N A N D P D

the emotional disturbances observed in PD, in orderto underline the functional roles of the dopaminergic pathways and basal ganglia (BG). The present review 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 the functional role of the striato-thalamo-cortical circuits in emotional processing.

Literature Review: Search Strategy and Selection CriteriaWe conducted a detailed search of the literature, with the aim of reviewing all the relevant papers on emotional processing and PD. The databases were selected using PubMed services with the following keywords: Parkinson’s disease, emotion, facial expression, emotional prosody, subjective feeling, arousal. Studies dealing with the emotional effects 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 STN’s functional role in emotional processing in general than about the speci- ficity of this processing in PD. We also hand searched all the relevant journals. In addition, we examined the bibliographies of key articles to glean further publica- tions. Our search was restricted to English-language papers and spanned the period from January 1990 to January 2010. Forty-three articles were identified as being relevant to the question of emotional processing in PD. No English-language papers exploring emotional processing in PD patients without DBS were excluded from the present review.

Emotional Processing in PDResearchers have reported deficits in several emotional components and processes in PD patients. These include not only changes in the emotional experience associating subjective feeling with physiological arousal, but also the impaired production and recognition of emotions conveyed by faces or voices. The results of these studies are summarized in Table 1.13–58

Subjective Feeling and Physiological Arousal

Emotional experience in PD has been investigated using emotional induction procedures generally associated with physiological measures. Participants are shown stimuli with a positive, negative, or neutral valence (eg, pictures from the International Affective Pic- ture System13,15,16 or words with emotional connotations14) and are then asked to self-report valence and physiological arousal.

Wieser et al.16 also carried out electroencephalography recordings during the rapid presentation of emo-

tionally charged pictures. PD patients reported a lowerlevel of physiological arousal than healthy controls (HC) for those items judged by the latter to induce the highest level of physiological arousal, which the authors ascribed to emotional blunting in PD. No difference, however, was found between the 2 groups of participants with respect to electroencephalography response patterns. These 2 sets of results were inter- preted as highlighting a dissociation between the early automatic processing of emotional information 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 physiological arousal and concomitant assessments of emotion were blunted, compared with those of the HC group using emotional words.

In Bowers et al.,13 a sudden noise was used to trig-

ger the eye-blink startle reflex (measured using electromyography) during stimulus presentation. Results showed that the startle reflex was selectively blunted in PD patients compared with HC in the aversive stimulus condition. This reflex was intact, however, in the positive- and neutral-valence conditions. To account for their results, the authors hypothesized that PD makes it harder for patients to gauge the threaten- ing value of negative stimuli, possibly due to reduced activation of the amygdala, a structure involved in

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 other types of aversive pictures was investigated by Miller et al.15 Results did not support the hypothesis of a specific deficit in emotional reactivity to fearful pictures, as PD patients also showed reduced reactivity to mutilation pictures, relative to other types of negative pictures. Further analyses revealed that startle eye-blink magnitude (measured while participants were viewing emotional stimuli) varied with arousal level in the HC, but not in the PD group. The authors suggested that decreased aversion-modulated startle might be driven by reduced reactivity to highly arousing negative stimuli, rather than to a specific category (ie, fear or disgust) of emotional stimuli.

These studies therefore seem to point to modifica- tions in both the ‘‘subjective feeling’’ and ‘‘physiological arousal’’ emotional components in PD. These have been linked to the difficulty encountered by PD patients in assessing their feelings on the basis of their physical and physiological sensations. Some authors, for instance, have claimed that PD patients suffer from alexithymia.59 Alexithymia is defined as the inability to identify and describe one’s feelings, and to distinguish between feelings and bodily sensations of emotional arousal.60

Movement Disorders, Vol. 27, No. 2, 2012 187

(2006)

(2007)

(2009)

(2008)

(1990)

TABLE 1. Overview of the clinical reports discussed in section 1 addressing the question of emotional processing in PD

Authors nDisease duration

DopaCognitive assessment

Depression AnxietyControl task

Emotional stimuli Dependent variables

Subjective feeling and arousal in Parkinson’s disease

Bowers et al.13 23 PD; 17 HC 9.9 6 5.9 years Yes Yes Yes No No Static pictures: Arousal (Likert); valence EMG; startle eye Arousal: PD < HC Severity (þ); depression(mean 6 SD) Neg, Pos, Neu (Likert) response (Neg); valence: PD (ns)

¼ HC; eye blink: PD

Hillier et al.14 8 PD; 15 HC 5–14 years (range) Yes No No No < HCYes Emotional words: Arousal (Likert); valence No Arousal and valence: PD NoNeg, Pos, Neu (Likert) < HC

Miller et al.15 24 PD; 24 HC 5.5 6 3.6 years Yes Yes Yes No No Static pictures: Arousal (Likert); Valence Startle eye blink Arousal and valence PD Sociodemographic,(mean 6 SD) Neg, Pos, Neu (Likert) < HC (Neg); startle clinical, and

Wieser et al.16 (2006)

14 PD; 14 HC 6.9 6 4.5 years(mean 6 SD)Yes No No No No Static pictures:

Neg, Pos, NeuArousal (Likert); valence(Likert)EEG Arousal: PD < HC; NoValence: PD ¼ HC; EEG: PD ¼ HCRecognition of facial expressions in Parkinson’s diseaseAdolphs et al.17 (1998)

18 PD; 13 HC 7.8 6 4.0 years(mean 6 SD)Yes Yes Yes No Yes Static faces: A, D,F, H, Neu, Sa, SCategorization; intensity(Likert)No Categorization andintensity: PD ¼ HCCategorization and matching: PD < HC (F and Sa)IQ, prosopagnosia,depression, gender (ns)/age (-)/education (þ)Depression executivefunctions, nonverbal IQ, motor and duration (ns)Ariatti et al.18 27 PD; 68 HC 1–13 years (range) Yes Yes Yes No Yes Static faces: A, D,

F, H, Neu, SaBeatty et al.19 (1989)

43 PD; 27 HC 4.7 6 NA years(mean 6 SD)

Yes (exc.1)

Yes Yes No Yes Static faces: A, D,F, H, Neu, Sa,

Categorization No Categorization: PD <HC; control task: PD

< HCCategorization and matching: PD < HC

Discrimination andProsopagnosia, globalefficiency, education (þ)NoNoBlonder et al.20 21 PD; 17 HC NA Yes No No No Yes S

Static faces: H, Sa,(1989)

Borod et al.21

20 PD; 21 HC NA Yes No No No No A, F, D, NeuStatic faces: A, D,

Breitenstein et al.22 (1998)

7 H&Y I; 7H&Y II PD; 12 HC

44.0 6 28.9months (I); 62.46 29.5 months(II) (mean 6SD)F, H, Neu, Sa,

SYes Yes No No Yes Static faces: H, Sa,

A, F, NeucategorizationDiscrimination; categorizationREP; intermodalemotional taskcategorization: PD

(1996)

< HCDiscrimination and No categorization: StageII PD < HC;discrimination and categorization: stage I PD ¼ HCCaekebekeet al.23 (1991)

21 PD; 14 HC 5.5 6 NA years(mean 6 SD)Yes Yes No No No NA NA Speech production;

PEP/REPSpeech, RFE, REP: PD No¼ HC; PEP: PD<HCClark 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., SCategorization REP; interpersonal

problemCategorization: PD <HCDepression anxiety (þ)(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., ADiscrimination No Discrimination: PD ¼

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, NeuCategorization; intensity(Likert)No Categorization andintensity: PD < HCMotor, executivefunctions, depression, anxiety, visuospatial (ns)

TABLE 1. (Continued)Disease Cognitive Control

Authors n 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 (early); 8.3 6 Sa., A

advancedPD/13 HC4.9 years(advanced) (mean 6 SD)¼ HC; control task:early PD < HC;advanced PD < HCJacobs et al.28 (1995)

12 PD; 30 HC NA Yes Yes Yes No Yes Static faces: H, A,Sa, F, Neu

Discrimination; matching No Discrimination andmatching: 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 staticfaces: A, F, H, S, Sa, D17 PD; 21 HC NA Yes Yes Yes No Yes Static faces: A, F,

H, S, Sa, DCategorization REP/recognition of

emotions from verbal stimuliCategorization Tridimensional personality questionnairePD < HC (F, D)PD < HC (A)Sociodemographic,clinical, cognitive (ns)Prosopagnosia (þ); motor, depression (ns); personality

(2003)

anger score (þ)Lotze et al.31 (2009)

10 PD; 10 HC 12.8 6 4.1 years(mean 6 SD)Yes/(OFF-PET)Yes Yes No No Dynamic emotional

and nonemo-tional gestures (faces and upper half of

the body)Categorization; valence

(analogical scale)fMRI; 11C-PET PD < HC (recognition of emotional gesture);

PD ¼ HC (valence); PD: decrease in the L ventrolateral prefrontal cortex and the R temporal sulcus related to emotional gestures

Striatal dopaminetransporter and errors in recognition of emotional gesture (-); striatal dopamine transporter and activation in the left ventrolateral cortex (þ)Madeley et al.32 (1995)

9 PD; 9 HC NA Yes No Yes Yes Yes Normal and PDstatic faces: Sa, A, D, NeuDiscrimination;categorization; expressivity (Likert)PFE Categorization, discrimi- Nonation: PD ¼ HC; PD faces less expressive than normal facesPell andLeonard33 (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, DDiscrimination;categorization; intensity (Likert)Recognition ofemotions from verbal stimuli; REPDiscrimination,categorization, and intensity: PD ¼ HCMotor, severity (-)Sprengelmeyeret al.34 (2003)

16 PD (off);20 PD (on);20 HC3.0 6 2.6 years(off dopa); 9.36 4.6 years (on dopa) (mean 6 SD)Yes/No Yes Yes No Yes Static faces: A, F,

H, S, Sa, DCategorization No on PD < HC; off PD < NoHC (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)Yes Yes Yes No Yes Static faces: A, F,

H, S, Sa, DCategorization; intensity(Likert)No Categorization and in-tensity: PD < HC (D)Sociodemographic,cognitive, depression (ns) (PD)10 PD; 10 HC NA Yes/No No No No Yes Static faces: A, F Matching

Yip et al.37

56 bilateral7.2 6 4.0 yearsYes Yes No No No Static faces: H, Sa,Discrimination;the off dopa/partiallyrestored in on dopa condition; RT: PD ¼ HCREP Discrimination andClinical (ns); visuospatial

PD; 8 RPD; 64 HC

(bilateral PD);2.8 6 1.6

A, S, D, F categorization

years (R PD)(mean 6 SD)

Yoshimuraet al.38 (2005)

(1998)

9 PD; 10 HC NA Yes No No Yes No Static faces: F, S,Neu

Discrimination RT; ERP Discrimination: PD ¼ NoHC; RT: PD ¼ HC;ERP: response in parietal cortex in PD/ in amygdala andtemporal cortex in HC (F)(Continued )



Recognition of emotional prosody in Parkinson’s diseaseAriatti et al.18 (2008)

11 PD; 68 HC NA Yes Yes Yes No No Sentences: A, D, F,H, Sa

Discrimination;categorizationRFE; linguisticprosody discrimination and categorizationDiscrimination andcategorization: PD <HC all tasksCategorization: PD (intact and impairedDepression, executivefunctions, nonverbal IQ, motor, duration (ns)Clinical and sociodemographicBenke et al.39 22 cog. intact 9.8 6 6.0 years Yes Yes Yes No Yes Sentences: A, S,

PD; 26 (intact); 9.9 6 Sa, cheerfulcog.impairedPD; 18 HC4.5 years(impaired) (mean 6 SD)mixed) ¼ HC; cate-gorization: impaired PD < HC; categorization: intact PD ¼ HC(ns)Blonder et al.20 (1989)

21 PD; 17 HC NA Yes No No No No Sentences: H, Sa,puzzled, A

Categorization Linguistic prosodydiscrimination; syntactical comprehension; stress comprehension; PEP;

RFECategorization: PD < NoHC; linguistic discrimination PD ¼ HC; syntactical: PD¼ HC; Stress: PD <HCBorod et al.21 (1990)

20 PD; 21 HC NA Yes No No No No Sentences: H, Sa.,A, Neu

Discrimination;categorizationRFE; PFE; PEP Discrimination: PD ¼ NoHC; categorization PD < HCBreitensteinet al.22 (1998)

7 H&Y I/PD; 7H&Y II/PD; 12 HC

44.0 6 28.9months (I); 62.46 29.5 months(II) (mean 6SD)Yes Yes No No Yes Sentences: H, Sa.,

A, NeuDiscrimination;categorizationRFE; intermodalemotional taskDiscrimination and Nocategorization: stage II PD < HC;discrimination and categorization: stage I PD ¼ HCBreitensteinet al.40 (2001)

14 advancedPD; 6 earlyPD; 16 HC59.1 6 58.3months (adv.); 16.2 6 7.8months (early) (mean 6 SD)Yes(mod.);No (early)a

Yes Yes No Yes Congruent andincongruent sentences: H, Sa, A, NeuCategorization Pitch variation

manipulationCategorization: advanced

PD < HC (greater for incongruence);categorization: early PD ¼ HC; categorization: early ¼advanced PD; pitch: PD ¼ HCSociodemographic, cognitive, and clinical (ns)Caekebekeet al.23 (1991)

21 PD; 14 HC 5.5 6 NA years(mean 6 SD)Yes Yes No No No NA NA Production ofspeech; PEP; RFEREP: PD ¼ HC; Noproduction speech: PD ¼ HCClark 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,

SCategorization RFE interpersonal

problemCategorization: PD ¼HCDepression 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, sen-tences: A, D, F, Sa, Neu, H, SCategorization (pseudo-words and sentences); valence (analogical scale); intensity (analogical scale) (pseudowords only)RFE/recognition ofemotions from verbal stimuliCategorization ofsentences: PD ¼HC; categorization of pseudowords: PD < HC; valence: PD <HC; intensity: PD ¼HC; verbal stimuli: PD ¼ HCClinical (ns)Kan et al.29 (2002)

16 PD; 24 HC NA Yes Yes Yes No No Sentences: H, Sa,A, F, S, D

Categorization RFE/recognition ofemotions from verbal stimuliCategorization: PD ¼HCSociodemographic,clinical, cognitive (ns)

TABLE 1. (Continued)Authors nDiseaseduration DopaCognitiveassessment Depression AnxietyControltask Emotional stimuli Dependent variables Others Results Correlations

Lloyd42 (1999) 16 PD; 20 HC NA Yes Yes Yes No Yes First name: H, Sa,

Neu

Discrimination;categorizationLing. Prosody dis-crimination and categorizationDiscrimination: PD ¼ NoHC; categorization: PD < HC; linguistic discrimination andcategorization: PD ¼HCMitchell andBoucas43 (2009)

Sentences: H, Sa;nouns: H, D, Sa, FCategorization No PD ¼ HC Disease duration (-),

motor (-)33 PD; 33 HC 8.0 6 4.6 years

(mean 6 SD)Yes (exc.

3)Yes No No Yes

21 PD; 21 HC 3.9 6 1.9 years (mean 6 SD)

Yes (exc.1)

Yes Yes No Yes

(2003)

(1998)

(1990)

Pell andLeonard44 (2003)

(1996) 11 PD; 11 HC 8.0 6 NA years

(mean 6 SD)

Pseudowords: H, A,D, Sa, S

Yes Yes No No Yes Sentences/pseudo-words/filtered sentences (without seg- mental information): A, Sa, HDiscrimination;categorization; intensity (Likert)Discrimination; categorizationLinguistic prosodydiscrimination; recognition of emotions from verbal stimuli; RFEStresscomprehensionDiscrimination andcategorization: PD < HC; intensity: PD < HC (D, Sa)Discrimination and categorization: PD < HC; stress: PD ¼ HCCognitive, control (ns)(PD)NoSchroder 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, HPassive listening;categorizationEEG (passive); RT(categorization)Categorization: PD < NoHC; 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)

Yes No No No Yes NA Matching; discrimination Speech production;linguistic prosodyproduction; PEPPD < HC for all tasks NoVe´ lez-Feijoet al.47 (2008)

35 PD; 65 HC 6.9 6 4.2 years(mean 6 SD)Yes Yes Yes No No Sentences: A, Sa,

H, NeuCategorization No PD > HC Depression (þ)Yip et al.37

56 bilateral7.2 6 4.0 yearsYes Yes No No No Sentence: H, Sa, A,Discrimination;RFE Discrimination andClinical (ns); visuospatial

PD; 8 RPD; 64 HC

(bilateral PD)/2.8 6 1.6yrs (R

S, D, F

PD); (mean 6SD)

Production of emotional prosody in Parkinson’s diseaseBenke et al.39 22 cog. intact 9.8 6 6.0 years Yes Yes Yes No No Sentences: A, S,

PD; 26 (intact); 9.9 6 Sa, cheerfulcog. 4.5 years

impaired (impaired)PD/18 HC (mean 6 SD)

Blonder et al.20 (1989)

21 PD; 17 HC NA Yes No No No Yes NA: H, Sa, puzzled,A

Spontaneous prod.(accuracy and intensity); imitation (accuracy); independent raters: yesLinguistic prosodyproduction and repetition¼ HCSpontaneous production No and repetition: PD <HC; linguistic production PD < HC; linguistic repetition:PD ¼ HCBorod et al.21 20 PD; 21 HC NA Yes No No No No Sentences: H, S,

interest, Sa, F,D, NeuVoluntary prod. (accu-racy, intensity); independent raters: yesRFE; PFE; REP PD < HC No(Continued )

(2008)

(2006)

(1984)

(1998)

(1980)


Authors n duration Dopa assessment Depression Anxiety task Emotional stimuli

Buck and Duffy48 9 PD; 10 NA (1980) patients

NA No No No No Pictures (familiar people, scenic,

Caekebekeet al.23 (1991)

withsomatic pathology21 PD; 14 HC 5.5 6 NA years(mean 6 SD)unpleasant,

unusual)Yes Yes No No Yes NA; A, hesitating,

NeuVoluntary production;spontaneous production; independent raters: yesSpeech production;RFE; REPVoluntary: PD < HC No(anger); spontaneous: PD < HC; speech:PD ¼ HCFirst name: Neu,Sa, HVoluntary production;imitation; independent raters: noSpeech production Production: PD < HC; Noimitation: PD ¼ HC; speech: PD ¼ HCMo¨ bes et al.49 16 PD; 16 HC 4.8 6 5.5 years Yes Yes Yes No Yes

(mean 6 SD)Production of facial expressions in Parkinson’s diseaseVoluntary production(accuracy, intensity); independent raters: yesVoluntary production; independent raters: NASpeech production;aphasiaSpeech prod./ ling. Prosody prod./ REPAccuracy: PD < HC (A,D); intensity: PD <HCREP: PD < HC; speech: PD ¼ HC; linguistic prosody: PD < HCSociodemographic,clinical, cognitive (ns)NoPell et al.50 21 PD; 12 HC 3.9 6 1.9 years Yes (exc. Yes Yes No Yes Sentences: A, D, H,

(mean 6 SD) 1) Neu, Sa, SScott et al.46 28 PD; 28 HC 8.0 6 NA years Yes No No No Yes NA

(mean 6 SD)Borod et al.21 (1990)

20 PD; 21 HC NA NA No No No No Sentences: H, S,interest, Sa, F, D, NeuPosed PFE; independentraters: yesRFE/PFE/REP Posed PFE: PD < HC NoBowers et al.13 2006

12 PD; 12 HC 5.5 6 2.5 years(mean 6 SD)Yes Yes Yes No No No Posed PFE (H, D, F, Sa,A, and S); interraters agreement: no (automatic method)No Frequency and speed NoPFE: MP < HCSpontaneous PFE(intensity, Pos and Neg valence); independent raters: yesSocial andinterpersonal functioning

Intensity PFE: PD < HC;Pos emotions PFE:PD < HC; Negemotions PFE: PD >HCSocial functioning (þ)Brozgold et al.51 20 PD; 21 HC NA NA NA Yes Yes No Relate emotional

experience(pleasant or

Buck and Duffy48 9 PD; 10 con- NA No NA NA NA Nounpleasant)

Pictures (familiar

trol group(patients with somatic pathology)people, scenic,unpleasant, unusual)Spontaneous PFE;

(2004)

independent raters: yesPEP Spontaneous PFE: PD < No

HCJacobs et al.28 (1995)

11 PD; 17HC NA Yes Yes Yes No Yes NA Posed PFE (type andintensity); independent raters: yesRFE Intensity PFE: PD < HC;posed PFE: PD <HC for A and SaPerceptual and imagerytask (þ)Katsikitis andPilowsky52 (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 No Cartoons pictures Spontaneous PFE(frequency and intensity); independent raters: noYes No Yes No No Cartoons pictures Spontaneous PFE(frequency and intensity); independent raters: yesNo PD < HC for degree ofmouth opening andfrequency of smilingNo Intensity : PD < HC;frequency: PD < HCDepression (þ)Depression (þ)Madeley et al.32 (1995)

9 PD; 9 HC NA Yes No Yes Yes Yes Normal and PDstatic faces: Sa, A, D, NeuExpressivity (posed andmimicry) (Likert); independent raters: yesRFE Expressiveness: PD < No

HC(Continued )



Pitcairn et al.54

(1990)4 PD; 12 HC NA NA No Yes Yes No Interview Spontaneous and posed PFE;

independent

Saku andEllgring55 (1992)

Simons et al.56

24 PD; 24 HC 6.7 6 5.4 years(mean 6 SD)19 PD; 26 HC 54.8 6 42.28months (means6 SD)Yes No No No No Odors (pleasant,unpleasant)Yes Yes Yes No No Video clips(comics); social interactionraters: NDSpontaneous PFE; independent raters: yesSpontaneous PFE; posed PFE; imitation PFE (Likert); independent raters: yesPD < HC; posedsmiles: PD > HC;frequency of smiling: PD ¼ HCNo Spontaneous prod: PD< HC (for unpleasant odors)No Spontaneous RFE: PD <HC; intensity of posed PFE: PD < HC (except A)NoDisease duration, social context, subjectivefeeling (þ)Simons et al.57 (2003)

22 PD; 22patients with somatic pathology6.82 6 3.57 years(mean 6 SD)

Yes Yes Yes No No Odors (pleasant,unpleasant)

Spontaneous PFE; posedPFE; imitation PFE; rated by FACS; independent raters: yesNo Intensity: PD ¼ HC; Noposed, spontaneous and imitationfrequency: MP < HC

109

Smith et al.58 (1996)

12 PD; 12 HC 6 years (medianduration)

Yes Yes Yes No No Film excerpts: Sa,H, F, A, D, NeuSpontaneous PFE; posedPFE; rated by FACS; independent raters: yesNo Posed PFE: PD ¼ HC; Nospontaneous PFE: PD

< HCThe 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 the

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 components and stimuli: for the recognition of facial expression, we considered as a control task an evaluation of prosopagnosia, 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 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 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 study, and the correlations between emotional results and secondary variables.

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; early, early stage of PD; EEG, electroencephalography; EMG, electromyography; ERP, event related potential; exc., except; 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; ND, no data; Neg, negative; Neu, neutral; off, off dopa condition; on, on dopa condition; Pos, positive; PD, Parkinson’s disease; 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 expression; RT, reaction time; S, surprise; Sa, sadness; SD, standard deviation.

Recognition of Facial Expressionsand Emotional ProsodyWhereas researchers have fairly consistently reported a deficit in the recognition of emotion conveyed by the human voice (ie, emotional prosody) in PD,20–22,29,37,39–42,44,46,61 studies of emotional facial expression (EFE) recognition have yielded some partic- ularly ambivalent results. Whereas some authors have reported diminished EFE recognition in Parkinsonian individuals compared with HC,24,26,28–30,34–37,39 others have failed to demonstrate any difference at all between the two.17,22,25,32,33

The main aim of Gray and Tickle-Degnen’s62 recent

meta-analysis was to examine the influence of several potential moderators of emotion recognition abilities in PD in order to disentangle apparent discrepancies in results, notably for the facial modality. The authors identified 7 potential moderators. Three of these concerned aspects of the emotion recognition tasks used by researchers (stimulus modality, task type, and emotion displayed). The other 4 concerned the PD patients themselves (motor disability, depression status, performance on executive function and visuospatial ability tasks, and medication status). First of all, they found a robust link between PD and impaired recognition of emotion from faces and voices confirming the existing literature and indicating that the deficit in emotion recognition in PD is cross-modal (‘‘stimulus modality’’ factor). That said, the deficit appeared to be greater for the recognition of emotion from prosody than from facial expressions. The authors suggested 3 potential explanations for this finding. First, emotional prosody recognition may be more suscepti- ble to the reduction in working memory capacity that is often noted in PD. Second, the BG may play a more

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 more variance in attempts to detect group differences. As far as ‘‘task type’’ is concerned, results reported by Gray and Tikle-Degnen62 indicate that both facial expression and prosody identification and discrimination tasks bring to light greater deficits than rating tasks, though with contrasting patterns for facial expressions and prosody. Discrimination tasks reveal a significantly greater deficit in facial emotion recognition, and identification tasks a significantly greater deficit in prosodic emotion recognition. As far as the ‘‘emotion displayed’’ factor is concerned, Gray and Tickle-Deg- nen62 also observed that individuals with PD were more impaired in the recognition of negative emotions (anger, disgust, fear, and sadness) than in that of relatively positive emotions (happiness, surprise). Accord- ing to the authors, these results were not simply artifacts reflecting different levels of difficulty across

emotions. Regarding clinical factors, results firstshowed that, across studies, the level of emotion recognition impairment did not appear to be related either to the level of ‘‘motor disability’’ or to ‘‘depression status,’’ suggesting that motor disability (and/or depression) and the deficit in emotion recognition stem from different forms of brain pathology. As far as ‘‘executive functions and visuospatial deficits’’ are concerned, results showed that (1) the facial emotion recognition deficit in PD goes beyond a general deficit in face processing, and (2) there is a link between prosodic emotion recognition and working memory, suggesting that deficits in prosodic emotion recognition in PD stem partially from working memory constraints. Finally, as far as ‘‘medication status’’ is concerned, although the authors noted a larger impairment effect size among patients who were 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 be noted that this meta-analysis only investigated behavioral results, and did not touch on physiological results, as measured by functional magnetic resonance imaging (fMRI), for example. In an fMRI investigation of PD patients performing a task in which they had to match faces expressing anger or fear, patients were assessed both on and off dopaminergic medication. No behavioral difference in terms of EFE recognition abilities was found either between the on and off dopa conditions or between PD patients and HC. However, reduced amygdala activation was observed in patients in a hypodopaminergic state comparedwith HC. This lack of response was partially restored by dopamine repletion.36 Additionally, in an event- related potential study, diminished amygdala activity in response to the perception of fearful facial expressions was observed in medicated PD patients compared with HC.38

All in all, these results confirmed that PD is characterized by a deficit in the recognition of facial and vocal expressions, which we believe could be partially explained by amygdala dysfunction. It also strongly suggested that discrepancies in results were due to the heterogeneous clinical profiles of the PD patients included in these studies, illustrated in Table 1.

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 reaction times of facial muscles. As the disease progresses, the face becomes ‘‘frozen’’ and inexpressive. Amimia can have a negative impact on PD patients’ interpersonal relationships.65

Researchers have long been interested in the possible distinction between voluntary and spontaneous facial

movements, insofar as they are subtended by 2 differ-ent neural networks: the pyramidal tract and the BG network.66 In PD, researchers have long hypothesized that voluntary emotional movements are less affected than spontaneous activity. This hypothesis was vali- dated in the 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 patients displayed reduced expressiveness when watching these extracts. In the condition where facial expressions were produced on command (voluntary), there was no difference between the 2 groups. By con- 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 patients.56,57

As with the emotion recognition processes, several confounding factors can explain the apparent discrep- ancy in results for the emotional production modality. The first set of factors concerns aspects of the emotion production tasks used by researchers (stimulus modality, task type, and emotion displayed). The second set of factors concerns the characteristics of the PD patients themselves, including medication status, depression status,68,69 and cognitive deterioration (eg, dysexecutive syndrome) owing to the spread of the lesions to nondopaminergic pathways.12 The problem is that studies exploring the production of facial expressions vary considerably in their emotional methodology, as well as in the availability of clinical data (Table 1). For example, none of the studies of EFE production in PD controlled for the impact of cognitive impairment or dopamine repletion. Accordingly, even though several hypotheses can be put forward, it is difficult to compare these different studies in order to identify the root causes of their apparently discrep- ant results.

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.20,21,39,49,50 Its interpretation is still a matter of considerable debate, with some researchers arguing that it should be regarded as a purely motor, articulatory disorder,70 and others suggesting instead that it is an emotional deficit.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 motor prosodic condition, PD patients exhibited a significant reduction in the production of emotional prosody. The authors concluded that dysprosody in PD cannot be ascribed solely to an articulatory impairment.

Some authors have argued that the deficit in the production of facial and vocal emotional expressions explains the deficit in emotion recognition processes in PD. Their hypothesis is based on the ‘‘simulation theory,’’ whereby, through a process of ‘‘facial feed- back,’’ facial muscular activity can modulate emo-

tional experiences elicited by some external stimulus(ie, something other than one’s own facial actions).71 Therefore, individuals with PD may, at least in part, experience deficits in emotion recognition because they have a reduced ability to spontaneously mimic displays of emotion.

DiscussionSynthesis

We have found a large body of evidence pointing to the existence of emotional disorders in PD. These con- cern several components of emotion, including subjective feeling, physiological arousal, and motor expression, and several input modalities, namely emotional prosody, facial expressions, and verbal labels (ie, words with emotional connotations), 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 is manifests itself in the recognition of emotion from both faces and voices. How- ever, it seems to be greater for the recognition of emotion from prosody than for the recognition of emotion from facial expressions. Furthermore, PD patients are more impaired in the recognition of negative emotions (anger, disgust, fear, and sadness) than in the recognition of relatively positive emotions (happiness, surprise). Apparent discrepancies in results could be attributed to several confounding factors. The first set of factors concerns aspects of the emotional task (eg, instructions, stimulus modality, task type, and emotion displayed), whereas the second set of factors concerns characteristics of the PD patients themselves (medication status, depression status, and performance on cognitive and visuospatial ability tasks). The problem is that these studies, especially research on the production of emotions, vary so widely in the emotional methodology used by researchers, as well as in the clinical profile of the PD patients, that comparisons are well nigh impossible (Table 1).

Although the pathophysiological mechanisms sub- tending these emotional disorders in PD are still not fully understood, such disturbances may well arise from (1) disruption of amygdala function in PD and

(2) impairment of the dopaminergic pathways and/or the BG in emotional processing.

Disruption of Amygdala Function in PD

The amygdala’s involvement in emotional processing is now well documented in the literature.63 For this reason, presumed impairment of the amygdala in PD has been put forward as an explanation for the emotional disorders observed in this pathology36,38 and has been the focus of a number of studies72–75 (cf. infra). Neuropathological research findings support

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 the basolateral nucleus, with the most massive loss (approximately 30%) occurring in the cortical nucleus. This fi has since been confirmed in other investigations.72–75

Dopaminergic Pathways and Emotional ProcessingApart from the amygdala dysfunction hypothesis, the most widely held hypothesis is that dopamine

the thalamus, putamen, and head of the caudate nu-cleus has been found in response to emotional prosody processing.101–104 Recently, activity of the STN was also observed in response to vocal emotions.105

Compelling evidence that the BG are engaged in the processing of speech prosody has also been gathered from clinical sources. In a comparative lesion study, Cancelliere and Kertesz106 concluded that deficits in the recognition 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.106–108 In a recent lesion study featuring a

depletion of the mesolimbic pathway brings about adichotic listening paradigm, Grandjean et al.dem-

110

dysfunction of the limbic loop linking the BG to theorbitofrontal 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 inthe processes that enable vocally expressed emotion to reduce spatial extinction syndrome. Similar results demonstrating the functional role of the BG in emotional processing in nigrostriatal lesion patients have

From a neuroanatomical point of view, most of theregions targeted by the projection of dopaminergicbeen found not just in the vocal modalityfacial one, too.111

but in theneurons, especially those in the mesolimbic and meso-cortical 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 facilitate the selection of the most appropriate strategy for a given situation.79

The role of dopamine in emotional processes in humans can be tested by manipulating dopamine ago- nists and antagonists. For example, a study by Law- rence et al.80 demonstrated that EFE recognition for anger was diminished following the administration of a dopaminergic antagonist. Similarly, an fMRI study revealed that the activity of several limbic regions (amygdala, hippocampus, anterior cingulate cortex) during the perception of unpleasant images was reduced in HC who had been given a dopaminergic antagonist.81 These results have been confirmed by other fMRI studies using dopamine manipulations.82–84

Data suggesting dopamine involvement in emotional processes have come from other sources, too, notably clinical studies of patients with neurological patholo- gies resulting in disturbed dopaminergic systems. Emo- tional disorders have been reported not only in PD, but also in schizophrenia (for a review, see Edwards et al.85), autism,86–93 attention-deficit hyperactivity disorder,94–96 and Huntington’s disease.97–99

Basal 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 been documented in patient, lesion, and fMRI studies.100–103

Using fMRI, several studies have reported subcortical activation during emotional processing. Activity of

These data fit in well with observations that emo-tional processing is typically impaired in patients with BG degeneration due to Huntington’s disease,97,112 reinforcing the view that the BG play an essential part in systems devoted to emotional processes.

Thus, there is growing evidence in favor of the involvement of the BG in emotional processing, not only directly, but also through their connections with brain structures known to be involved in emotional processing.

ConclusionThe present review provides a synopsis of the emotional disturbances observed in PD. The disruption of several components of emotional processing does indeed point to the functional involvement of the dopaminergic pathways and BG in these processes. This review also underlines the need to control for potential confounding factors linked to the emotional tasks but also to the sociodemographic and clinical characteristics of the PD patients themselves. From a clinical point of view, the consequences of these emotional disturbances in daily living and their relationship to mood and behavioral disorders such as depression, anxiety and apathy, often observed in PD, remain to be clarified.

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 manuscript.

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and Marc Ve´ rin, MD, PhD1,2


tional disturbances observed in Parkinson’s disease. We then discuss the functional roles of the striato-thalamo- cortical and mesolimbic circuits, ending with the conclu- sion that both these pathways are indeed involved in emotional processing. VC 2011 Movement Disorder Society

episodes of synchronized changes in several of the organism’s components (including physiological arousal, motor expression, subjective feeling and, according to some researchers, action tendencies and cognitive processes as well) in response to environ- mental events of major significance to the organism. These events may be either internal (eg, thoughts, sensations, memories) or external (eg, other people’s behavior, a change of situation, an encounter with a novel stimulus).1–5 The concept of ‘‘physiological arousal’’ refers to the fact that different types of physi-

ological activation (autonomic nervous system, hor- mone levels, and certain neurotransmitters) are associated with emotional states.6 The concept of

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.

The concept of ‘‘subjective feeling’’ refers to the fact that, in humans, emotions are associated with an internal subjective state.8

This last definition encompasses several features that are deemed to be inseparable from emotion, in partic- ular its episodic nature9–11 and the idea that emotions are normally generated by events that have important meaning for the organism. In turn, these 2 features underline the 2 main differences between affective states (such as mood) and emotions, namely: (1) duration (ie, mood lasts longer than emotion) and (2) the presence or absence of an external/internal event (ie, mood does not necessarily have to have a trigger).

Parkinson’s disease (PD) constitutes a useful model for studying the neural substrates of emotional processing. Even if PD involves multiple neuronal systems,12 PD is histopathologically characterized by selective, progressive, and chronic degeneration of the nigrostriatal and mesocorticolimbic dopamine systems, and offers an opportunity to study the possible influence of these dopaminergic pathways on emotional processing.

to underline the functional roles of the dopaminergic pathways and basal ganglia (BG). The present review 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 the functional role of the striato-thalamo-cortical circuits in emotional processing.

We conducted a detailed search of the literature, with the aim of reviewing all the relevant papers on emotional processing and PD. The databases were selected using PubMed services with the following keywords: Parkinson’s disease, emotion, facial expression, emotional prosody, subjective feeling, arousal. Studies dealing with the emotional effects 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 STN’s functional role in emotional processing in general than about the speci- ficity of this processing in PD. We also hand searched all the relevant journals. In addition, we examined the bibliographies of key articles to glean further publica- tions. Our search was restricted to English-language papers and spanned the period from January 1990 to January 2010. Forty-three articles were identified as being relevant to the question of emotional processing in PD. No English-language papers exploring emotional processing in PD patients without DBS were excluded from the present review.

Researchers have reported deficits in several emotional components and processes in PD patients. These include not only changes in the emotional experience associating subjective feeling with physiological arousal, but also the impaired production and recognition of emotions conveyed by faces or voices. The results of these studies are summarized in Table 1.13–58


level of physiological arousal than healthy controls (HC) for those items judged by the latter to induce the highest level of physiological arousal, which the authors ascribed to emotional blunting in PD. No difference, however, was found between the 2 groups of participants with respect to electroencephalography response patterns. These 2 sets of results were inter- preted as highlighting a dissociation between the early automatic processing of emotional information 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 physiological arousal and concomitant assessments of emotion were blunted, compared with those of the HC group using emotional words.


The question of whether this reduced reactivity to emotional stimuli is driven by diminished reactivity to fear-eliciting stimuli as opposed to other types of aversive pictures was investigated by Miller et al.15 Results did not support the hypothesis of a specific deficit in emotional reactivity to fearful pictures, as PD patients also showed reduced reactivity to mutilation pictures, relative to other types of negative pictures. Further analyses revealed that startle eye-blink magnitude (measured while participants were viewing emotional stimuli) varied with arousal level in the HC, but not in the PD group. The authors suggested that decreased aversion-modulated startle might be driven by reduced reactivity to highly arousing negative stimuli, rather than to a specific category (ie, fear or disgust) of emotional stimuli.


Overview of the clinical reports discussed in section 1 addressing the question of emotional processing in PD

Dependent variables Others Results Correlations

No Static pictures: Arousal (Likert); valence EMG; startle eye Arousal: PD < HC Severity (þ); depressionNeg, Pos, Neu (Likert) response (Neg); valence: PD (ns)¼ HC; eye blink: PD

Yes Emotional words: Arousal (Likert); valence No Arousal and valence: PD NoNeg, Pos, Neu (Likert) < HCNo Static pictures: Arousal (Likert); Valence Startle eye blink Arousal and valence PD Sociodemographic,Neg, Pos, Neu (Likert) < HC (Neg); startle clinical, and

eye blink did not neuropsychologicalvary by arousal level variables (ns)(PD) as is the casein HC

Categorization; matching REP

Categorization; matching PEP; REP

Discrimination; REP; PEP; PFE


Discrimination No Discrimination early PD Cognitive, visuospatial,

¼ HC; advanced PD clinical (ns) (PD)

RT; BOLD fMRI Matching: on PD < HC; Nooff PD < HC; bilat-eral amygdala response absent in

categorization categorization:bilateral PD < HC;

(þ)

discrimination: rightPD ¼ HD;categorization right

PD < HC


Categorization PEP

categorization categorization:bilateral PD < HC;

(þ)

discrimination: R PD¼ HC; categorization: R PD < HC

Voluntary production REP Production: PD (intact Education, speed index(accuracy); i and impaired mixed) (þ); Others clinical,ndependent raters: < HC; production: cognitive andyes impaired PD < HC; sociodemographic

production: intact PD (ns)


Spontaneous PEP; independent raters: yes

PFE Spontaneous PEP: PD < No HC


Spontaneous and posed PFE; independent

Gestures and posture

Expressiveness: PD <HC; happy smiles:

No

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 the


No 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; early, early stage of PD; EEG, electroencephalography; EMG, electromyography; ERP, event related potential; exc., except; 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; ND, no data; Neg, negative; Neu, neutral; off, off dopa condition; on, on dopa condition; Pos, positive; PD, Parkinson’s disease; 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 expression; RT, reaction time; S, surprise; Sa, sadness; SD, standard deviation.

Whereas researchers have fairly consistently reported a deficit in the recognition of emotion conveyed by the human voice (ie, emotional prosody) in PD,20–22,29,37,39–42,44,46,61 studies of emotional facial expression (EFE) recognition have yielded some partic- ularly ambivalent results. Whereas some authors have reported diminished EFE recognition in Parkinsonian individuals compared with HC,24,26,28–30,34–37,39 others have failed to demonstrate any difference at all between the two.17,22,25,32,33


meaning that tests 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 Tikle-Degnen62 indicate that both facial expression and prosody identification and discrimination tasks bring to light greater deficits than rating tasks, though with contrasting patterns for facial expressions and prosody. Discrimination tasks reveal a significantly greater deficit in facial emotion recognition, and identification tasks a significantly greater deficit in prosodic emotion recognition. As far as the ‘‘emotion displayed’’ factor is concerned, Gray and Tickle-Deg- nen62 also observed that individuals with PD were more impaired in the recognition of negative emotions (anger, disgust, fear, and sadness) than in that of relatively positive emotions (happiness, surprise). Accord- ing to the authors, these results were not simply artifacts reflecting different levels of difficulty across

showed that, across studies, the level of emotion recognition impairment did not appear to be related either to the level of ‘‘motor disability’’ or to ‘‘depression status,’’ suggesting that motor disability (and/or depression) and the deficit in emotion recognition stem from different forms of brain pathology. As far as ‘‘executive functions and visuospatial deficits’’ are concerned, results showed that (1) the facial emotion recognition deficit in PD goes beyond a general deficit in face processing, and (2) there is a link between prosodic emotion recognition and working memory, suggesting that deficits in prosodic emotion recognition in PD stem partially from working memory constraints. Finally, as far as ‘‘medication status’’ is concerned, although the authors noted a larger impairment effect size among patients who were 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 be noted that this meta-analysis only investigated behavioral results, and did not touch on physiological results, as measured by functional magnetic resonance imaging (fMRI), for example. In an fMRI investigation of PD patients performing a task in which they had to match faces expressing anger or fear, patients were assessed both on and off dopaminergic medication. No behavioral difference in terms of EFE recognition abilities was found either between the on and off dopa conditions or between PD patients and HC. However, reduced amygdala activation was observed in patients in a hypodopaminergic state comparedAdditionally, in an event- related potential study, diminished amygdala activity in response to the perception of fearful facial expressions was observed in medicated PD patients compared with HC.38



In PD, researchers have long hypothesized that voluntary emotional movements are less affected than spontaneous activity. This hypothesis was vali- dated in the 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 patients displayed reduced expressiveness when watching these extracts. In the condition where facial expressions were produced on command (voluntary), there was no difference between the 2 groups. By con- 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 patients.56,57


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.20,21,39,49,50 Its interpretation is still a matter of considerable debate, with some researchers arguing that it should be regarded as a purely motor, articulatory disorder,70 and others suggesting instead that it is an emotional deficit.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 motor prosodic condition, PD patients exhibited a significant reduction in the production of emotional prosody. The authors concluded that dysprosody in PD cannot be ascribed solely to an articulatory impairment.


Therefore, individuals with PD may, at least in part, experience deficits in emotion recognition because they have a reduced ability to spontaneously mimic displays of emotion.


Although the pathophysiological mechanisms sub- tending these emotional disorders in PD are still not fully understood, such disturbances may well arise from (1) disruption of amygdala function in PD and

For this reason, presumed impairment of the amygdala in PD has been put forward as an explanation for the emotional disorders observed in this pathology36,38 and has been the focus of a number of studies72–75 (cf. infra). Neuropathological research findings support

carried out postmortem examinations of nondemented PD patients and reported a signifi reduction in the neuron density of the basolateral nucleus, with the most massive loss (approximately 30%) occurring in the cortical nucleus. This fi has since been confirmed in other investigations.72–75

Recently, activity of the STN was also observed in response to vocal emotions.105

Compelling evidence that the BG are engaged in the processing of speech prosody has also been gathered from clinical sources. In a comparative lesion study, Cancelliere and Kertesz106 concluded that deficits in the recognition 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.106–108 In a recent lesion study featuring a

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).

the processes that enable vocally expressed emotion to reduce spatial extinction syndrome. Similar results demonstrating the functional role of the BG in emotional processing in nigrostriatal lesion patients have

Data from animal experiments also highlight the involvement of dopamine in emotional processes and suggest that dopaminergic neurons facilitate the selection of the most appropriate strategy for a given situation.79

The role of dopamine in emotional processes in humans can be tested by manipulating dopamine ago- nists and antagonists. For example, a study by Law- rence et al.80 demonstrated that EFE recognition for anger was diminished following the administration of a dopaminergic antagonist. Similarly, an fMRI study revealed that the activity of several limbic regions (amygdala, hippocampus, anterior cingulate cortex) during the perception of unpleasant images was reduced in HC who had been given a dopaminergic antagonist.81 These results have been confirmed by other fMRI studies using dopamine manipulations.82–84


The studies reporting emotional disturbance in PD cited herein point to the involvement of the BG in emotional processing, which has also been documented in patient, lesion, and fMRI studies.100–103

97,112 reinforcing the view that the BG play an essential part in systems devoted to emotional processes.

Thus, there is growing evidence in favor of the involvement of the BG in emotional processing, not only directly, but also through their connections with brain structures known to be involved in emotional processing.

The present review provides a synopsis of the emotional disturbances observed in PD. The disruption of several components of emotional processing does indeed point to the functional involvement of the dopaminergic pathways and BG in these processes. This review also underlines the need to control for potential confounding factors linked to the emotional tasks but also to the sociodemographic and clinical characteristics of the PD patients themselves. From a clinical point of view, the consequences of these emotional disturbances in daily living and their relationship to mood and behavioral disorders such as depression, anxiety and apathy, often observed in PD, remain to be clarified.

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tional disturbances observed in Parkinson’s disease. We then discuss the functional roles of the striato-thalamo- cortical and mesolimbic circuits, ending with the conclu- sion that both these pathways are indeed involved in emotional processing. VC 2011 Movement Disorder Society


and the idea that emotions are normally generated by events that have important meaning for the organism. In turn, these 2 features underline the 2 main differences between affective states (such as mood) and emotions, namely: (1) duration (ie, mood lasts longer than emotion) and (2) the presence or absence of an external/internal event (ie, mood does not necessarily have to have a trigger).

PD is histopathologically characterized by selective, progressive, and chronic degeneration of the nigrostriatal and mesocorticolimbic dopamine systems, and offers an opportunity to study the possible influence of these dopaminergic pathways on emotional processing.

to underline the functional roles of the dopaminergic pathways and basal ganglia (BG). The present review 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 the functional role of the striato-thalamo-cortical circuits in emotional processing.






Results did not support the hypothesis of a specific deficit in emotional reactivity to fearful pictures, as PD patients also showed reduced reactivity to mutilation pictures, relative to other types of negative pictures. Further analyses revealed that startle eye-blink magnitude (measured while participants were viewing emotional stimuli) varied with arousal level in the HC, but not in the PD group. The authors suggested that decreased aversion-modulated startle might be driven by reduced reactivity to highly arousing negative stimuli, rather than to a specific category (ie, fear or disgust) of emotional stimuli.




studies of emotional facial expression (EFE) recognition have yielded some partic- ularly ambivalent results. Whereas some authors have reported diminished EFE recognition in Parkinsonian individuals compared with HC,24,26,28–30,34–37,39 others have failed to demonstrate any difference at all between the two.17,22,25,32,33


meaning that tests 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 Tikle-Degnen62 indicate that both facial expression and prosody identification and discrimination tasks bring to light greater deficits than rating tasks, though with contrasting patterns for facial expressions and prosody. Discrimination tasks reveal a significantly greater deficit in facial emotion recognition, and identification tasks a significantly greater deficit in prosodic emotion recognition. As far as the ‘‘emotion displayed’’ factor is concerned, Gray and Tickle-Deg- nen62 also observed that individuals with PD were more impaired in the recognition of negative emotions (anger, disgust, fear, and sadness) than in that of relatively positive emotions (happiness, surprise). Accord- ing to the authors, these results were not simply artifacts reflecting different levels of difficulty across

showed that, across studies, the level of emotion recognition impairment did not appear to be related either to the level of ‘‘motor disability’’ or to ‘‘depression status,’’ suggesting that motor disability (and/or depression) and the deficit in emotion recognition stem from different forms of brain pathology. As far as ‘‘executive functions and visuospatial deficits’’ are concerned, results showed that (1) the facial emotion recognition deficit in PD goes beyond a general deficit in face processing, and (2) there is a link between prosodic emotion recognition and working memory, suggesting that deficits in prosodic emotion recognition in PD stem partially from working memory constraints. Finally, as far as ‘‘medication status’’ is concerned, although the authors noted a larger impairment effect size among patients who were 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 be noted that this meta-analysis only investigated behavioral results, and did not touch on physiological results, as measured by functional magnetic resonance imaging (fMRI), for example. In an fMRI investigation of PD patients performing a task in which they had to match faces expressing anger or fear, patients were assessed both on and off dopaminergic medication. No behavioral difference in terms of EFE recognition abilities was found either between the on and off dopa conditions or between PD patients and HC. However, reduced amygdala activation was observed in patients in a hypodopaminergic state comparedAdditionally, in an event- related potential study, diminished amygdala activity in response to the perception of fearful facial expressions was observed in medicated PD patients compared with HC.38



In PD, researchers have long hypothesized that voluntary emotional movements are less affected than spontaneous activity. This hypothesis was vali- dated in the 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 patients displayed reduced expressiveness when watching these extracts. In the condition where facial expressions were produced on command (voluntary), there was no difference between the 2 groups. By con- 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 patients.56,57


Its interpretation is still a matter of considerable debate, with some researchers arguing that it should be regarded as a purely motor, articulatory disorder,70 and others suggesting instead that it is an emotional deficit.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 motor prosodic condition, PD patients exhibited a significant reduction in the production of emotional prosody. The authors concluded that dysprosody in PD cannot be ascribed solely to an articulatory impairment.


Therefore, individuals with PD may, at least in part, experience deficits in emotion recognition because they have a reduced ability to spontaneously mimic displays of emotion.


For this reason, presumed impairment of the amygdala in PD has been put forward as an explanation for the emotional disorders observed in this pathology36,38 and has been the focus of a number of studies72–75 (cf. infra). Neuropathological research findings support

carried out postmortem examinations of nondemented PD patients and reported a signifi reduction in the neuron density of the basolateral nucleus, with the most massive loss (approximately 30%) occurring in the cortical nucleus. This fi has since been confirmed in other investigations.72–75

concluded that deficits in the recognition 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.106–108 In a recent lesion study featuring a

demonstrated that EFE recognition for anger was diminished following the administration of a dopaminergic antagonist. Similarly, an fMRI study revealed that the activity of several limbic regions (amygdala, hippocampus, anterior cingulate cortex) during the perception of unpleasant images was reduced in HC who had been given a dopaminergic antagonist.81 These results have been confirmed by other fMRI studies using dopamine manipulations.82–84



72. Ouchi Y, Yoshikawa E, Okada H, et al. Alterations in binding site density of dopamine transporter in the striatum, orbitofrontal cortex, and amygdala in early Parkinson’s disease: compartment analysis for beta-CFT binding with positron emission tomography. Ann Neurol 1999;45:601–610.




PD is histopathologically characterized by selective, progressive, and chronic degeneration of the nigrostriatal and mesocorticolimbic dopamine systems, and offers an opportunity to study the possible influence of these dopaminergic pathways on emotional processing.



) and are then asked to self-report valence and physiological arousal.







studies of emotional facial expression (EFE) recognition have yielded some partic- ularly ambivalent results. Whereas some authors have reported diminished EFE recognition in Parkinsonian individuals compared with HC,24,26,28–30,34–37,39 others have failed to demonstrate any difference at all between the two.17,22,25,32,33


indicate that both facial expression and prosody identification and discrimination tasks bring to light greater deficits than rating tasks, though with contrasting patterns for facial expressions and prosody. Discrimination tasks reveal a significantly greater deficit in facial emotion recognition, and identification tasks a significantly greater deficit in prosodic emotion recognition. As far as the ‘‘emotion displayed’’ factor is concerned, Gray and Tickle-Deg- nen62 also observed that individuals with PD were more impaired in the recognition of negative emotions (anger, disgust, fear, and sadness) than in that of relatively positive emotions (happiness, surprise). Accord- ing to the authors, these results were not simply artifacts reflecting different levels of difficulty across

showed that, across studies, the level of emotion recognition impairment did not appear to be related either to the level of ‘‘motor disability’’ or to ‘‘depression status,’’ suggesting that motor disability (and/or depression) and the deficit in emotion recognition stem from different forms of brain pathology. As far as ‘‘executive functions and visuospatial deficits’’ are concerned, results showed that (1) the facial emotion recognition deficit in PD goes beyond a general deficit in face processing, and (2) there is a link between prosodic emotion recognition and working memory, suggesting that deficits in prosodic emotion recognition in PD stem partially from working memory constraints. Finally, as far as ‘‘medication status’’ is concerned, although the authors noted a larger impairment effect size among patients who were 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 be noted that this meta-analysis only investigated behavioral results, and did not touch on physiological results, as measured by functional magnetic resonance imaging (fMRI), for example. In an fMRI investigation of PD patients performing a task in which they had to match faces expressing anger or fear, patients were assessed both on and off dopaminergic medication. No behavioral difference in terms of EFE recognition abilities was found either between the on and off dopa conditions or between PD patients and HC. However, reduced amygdala activation was observed in patients in a hypodopaminergic state compared


which showed that although PD patient and HC groups assessed the emotional intensity of video clips in the same way, the PD patients displayed reduced expressiveness when watching these extracts. In the condition where facial expressions were produced on command (voluntary), there was no difference between the 2 groups. By con- 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 patients.56,57


and others suggesting instead that it is an emotional deficit.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 motor prosodic condition, PD patients exhibited a significant reduction in the production of emotional prosody. The authors concluded that dysprosody in PD cannot be ascribed solely to an articulatory impairment.


(cf. infra). Neuropathological research findings support

concluded that deficits in the recognition 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.106–108 In a recent lesion study featuring a


), autism,86–93 attention-deficit hyperactivity disorder,94–96 and Huntington’s disease.97–99








Alexithymia is defined as the inability to identify and describe one’s feelings, and to distinguish between feelings and bodily sensations of emotional arousal.60


, on dopa condition; Pos, positive; PD, Parkinson’s disease; 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 expression; RT, reaction time; S, surprise; Sa, sadness; SD, standard deviation.

others have failed to demonstrate any difference at all between the two.17,22,25,32,33





and cognitive deterioration (eg, dysexecutive syndrome) owing to the spread of the lesions to nondopaminergic pathways.12 The problem is that studies exploring the production of facial expressions vary considerably in their emotional methodology, as well as in the availability of clinical data (Table 1). For example, none of the studies of EFE production in PD controlled for the impact of cognitive impairment or dopamine repletion. Accordingly, even though several hypotheses can be put forward, it is difficult to compare these different studies in order to identify the root causes of their apparently discrep- ant results.

who found that although PD and HC did not differ in a nonemotional motor prosodic condition, PD patients exhibited a significant reduction in the production of emotional prosody. The authors concluded that dysprosody in PD cannot be ascribed solely to an articulatory impairment.



supported this interpretation, in that the PD patients’ self-reports of physiological arousal and concomitant assessments of emotion were blunted, compared with those of the HC group using emotional words.



, on dopa condition; Pos, positive; PD, Parkinson’s disease; 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 expression; RT, reaction time; S, surprise; Sa, sadness; SD, standard deviation.





The problem is that studies exploring the production of facial expressions vary considerably in their emotional methodology, as well as in the availability of clinical data (Table 1). For example, none of the studies of EFE production in PD controlled for the impact of cognitive impairment or dopamine repletion. Accordingly, even though several hypotheses can be put forward, it is difficult to compare these different studies in order to identify the root causes of their apparently discrep- ant results.



These results have been confirmed by other fMRI studies using dopamine manipulations.82–84



supported this interpretation, in that the PD patients’ self-reports of physiological arousal and concomitant assessments of emotion were blunted, compared with those of the HC group using emotional words.





or in both spontaneous EFE and voluntary EFE production in PD patients.56,57





also observed that individuals with PD were more impaired in the recognition of negative emotions (anger, disgust, fear, and sadness) than in that of relatively positive emotions (happiness, surprise). Accord- ing to the authors, these results were not simply artifacts reflecting different levels of difficulty across





dopa conditions. It should be noted that this meta-analysis only investigated behavioral results, and did not touch on physiological results, as measured by functional magnetic resonance imaging (fMRI), for example. In an fMRI investigation of PD patients performing a task in which they had to match faces expressing anger or fear, patients were assessed both on and off dopaminergic medication. No behavioral difference in terms of EFE recognition abilities was found either between the on and off dopa conditions or between PD patients and HC. However, reduced amygdala activation was observed in patients in a hypodopaminergic state compared



dopaminergic medication. No behavioral difference in terms of EFE recognition abilities was found either between the on and off dopa conditions or between PD patients and HC. However, reduced amygdala activation was observed in patients in a hypodopaminergic state compared


dopa conditions or between PD patients and HC. However, reduced amygdala activation was observed in patients in a hypodopaminergic state compared


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