18 Saenz Leandro - Calder

Neuropsychologia 48 (2010) 27192729

Contents lists available at ScienceDirect

Neuropsychologia

journa l homepage: www.e lsev ier .com/ loca

The rel s oemotio on

Andrew w DRoger A.a MRC Cognitiob Department oc Wales Institut ark Pld Cambridge Ce

a r t i c l

Article history:Received 8 SepReceived in revised form 4 May 2010Accepted 10 May 2010Available online 16 May 2010

Keywords:Huntingtons dAngerDisgustEmotionFacial expressVocal expressiStriatumInsula

in Huin recognising disgust. Not all subsequent studies have found this pattern, and a review of the literatureto date shows that marked impairments in recognising anger are also often seen in HD. However, themajority of studies have based their conclusions on a single test of facial expression recognition. In thecurrent study we revisit this issue of emotion recognition in HD to address whether the pattern found onone test of facial expression recognition generalised to another, and to different modalities using tests ofemotion recognition from facial expressions, vocal expressions, and short verbal vignettes. The results

1. Introdu

Huntingclassically rpsychiatricatric impairaltered behstates (Crau

Sprengerecognitionpromised iless severeparticular ainvestigatinifest HD (Wby Montagn

CorresponE-mail add

0028-3932/$ doi:10.1016/j.isease

ionsons

showed evidence of impairments in recognising anger, fear and disgust across the three domains, withrecognition of anger the most severely impaired. Given work identifying different subtypes of disgustthat are associatedwith different facial features, a second study examined the recognition of three disgustexpressions that healthy participants reliably associate with unpleasant tastes, unpleasant smells, anda more general elaborated or expanded form of disgust that includes reactions to violations of moralstandards. The results showed a disproportionate impairment in recognising faces associated with theexpanded form, the subtype most closely aligned with anger. We conclude that the related emotions ofdisgust and anger associated with social disapproval are frequently impaired in HD and discuss factorsthat might cause one emotion to show more severe impairments than the other.

2010 Elsevier Ltd. All rights reserved.

ction

tons disease (HD) is a trinucleotide repeat disorder thatesults in cognitive impairments, motor disorders, andand emotional symptoms. The emotional and psychi-ments have adramatic impact on family life and includeaviour and impaired interpretation of others emotionalfurd & Snowden, 2002). Here we focus on the latter.lmeyer et al. (1996) were the rst to report that theof facial expressions of disgust was particularly com-

n patients with manifest HD, although marked butimpairments were also found for other emotions, innger and fear. Similar results were found in a studyg a small group (n=6) of Chinese patients with man-ang, Hoosain, Yang, Meng, & Wang, 2003). A third studye et al. (2006) found impaired recognition of disgust

ding author. Tel.: +44 1223 355 294x750; fax: +44 1223 359 062.ress: [email protected] (A.J. Calder).

and anger from animated sequences of morphed facial expressionsranging between neutral and each of six target expressions; how-ever, the anger decit was restricted to low-intensity morphs anddisgust alone was impaired for sequences ranging between neutraland 100% of the target emotions.

Not all studieshave foundevidenceof adisproportionatedisgustdecit in manifest patients, however. Milders, Crawford, Lamba,and Simpson (2003) found impairments for facial expressions ofanger, fear, disgust, and sadness, but there was no evidence thatthe disgust decit was more severe, and fear showed a more severeimpairment than disgust. More recently, Henley et al. (2008) andSnowden et al. (2008) have found disproportionate impairments inrecognising angry facial expressions.

Less severe but more selective disgust impairments have beenfound in premanifest individuals that tested positive for theHD gene mutation (Gray, Young, Barker, Curtis, & Gibson, 1997;Hennenlotter et al., 2004; Sprengelmeyer, Schroeder, Young, &Epplen, 2006). Some of these studies compared a group of pre-manifest gene positive individuals with their partners or a groupof gene negative at-risk individuals (Gray et al., 1997; Henley

see front matter 2010 Elsevier Ltd. All rights reserved.neuropsychologia.2010.05.019ation between anger and different formn recognition impairments in Huntingt

J. Caldera,, Jill Keanea, Andrew W. Youngb, AndreBarkerd

n and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 7EF, UKf Psychology, University of York, Heslington, York YO10 5DD, UKe of Cognitive Neuroscience, School of Psychology, Cardiff University, Tower Building, Pntre for Brain Repair, Forvie Site, Addenbrookes Hosptial, Cambridge, UK

e i n f o

tember 2009

a b s t r a c t

Initial reports of emotion recognitionte /neuropsychologia

f disgust: Implications fors disease

. Lawrencec, Sarah Masond,

ace CF10 3AT, UK

ntingtons disease (HD) found disproportionate impairments

2720 A.J. Calder et al. / Neuropsychologia 48 (2010) 27192729

et al., 2008; Johnson et al., 2007; Kipps, Duggins, McCusker, &Calder, 2007; Sprengelmeyer et al., 2006). In other studies thecontrols were unrelated, healthy, neurologically intact individuals(Hennenlotter et al., 2004; Milders et al., 2003). The clearest evi-dence of a dwho foundthree separmonths. On(surprise) imnition of diset al., 1997al. (2004) ausing the on

As in thpremanifesrecognizinget al., 2003borderline imore interemanifest HDin the ante(VBM) (Kipatedwithwusing fMRIactivation tndings accinsula in dis2007; Philliing (Krolak(Adolphs, TYoung, 200

In the lafest HD to drecognitionfor the genshowed impdisgust, feaproportionadivided intdisorder exUHDRS; Kiethat any monly emotigroup (minrecognitionat recognisisubgroupsresponse tianger for asubgroup, whappy expr

The absedisgust intion of facidemonstratmany otherropsychiatrvariability iuals (Craufuclear that wpass more tMoreover,disgust andtionate ang

These colargely on

he Citerms

sell (1

nd coch tto der vationoweinvexpreyes,gustelmet faciemo

ed retion(Ha

ds (2egen, 1997). Hayes et al. (2007) also demonstrated impairedto conceptual knowledge of disgust in the form of fewerted examples of disgust situations and impaired identica-disgust from pictures of emotional scenes. However, in addressing emotion recognition from facial and vocal signalserwith emotion recognition fromverbal scenarios, Snowden(2008) found the most consistent impairments for anger.rly, an investigation of emotion from animated bodies, thatt include stimuli depicting disgust, reported impaired recog-of anger (de Gelder, Van den Stock, de Diego Balaguer, &d-Lvi, 2008).rom cues other than faces, there is initial evidence that dis-d anger show evidence of disproportionate impairments. It

efore of note that these two emotions are often confused, aat is reectedby their proximal locations in two-dimensionals of emotion, such as Russells (1980). Circumplex modelch emotions are coded in terms of the degree to whichoke arousal and their relative pleasantness/unpleasantness.he current study, we revisited the issue of emotion recog-in manifest HD patients. Since the majority of studies haveted emotion recognition using a single test, we addressedisgust impairment is from Sprengelmeyer et al. (2006)impaired recognition of facial expressions of disgust onate testing sessions, separated by approximately 67ly on the third occasion was another facial expressionpaired. Other studies have also found impaired recog-

gust in asymptomatic Huntingtons participants (Gray; Hennenlotter et al., 2004); although Hennenlotter etlso found a borderline impairment for anger (p=0.052)e-tailed criterion they applied to the disgust contrast.e case of manifest HD, not all studies investigatingt individuals have found disproportionate problems indisgust (Henley et al., 2008; Kipps et al., 2007; Milders). The only effect found by Kipps et al. (2007) was ampairment for facial expressions of anger. However, ofst, they demonstrated that disgust recognition in pre-was signicantly correlated with grey matter volume

rior insula estimated using voxel-based morphometryps et al., 2007), with decreasing insula volume associ-orse recognition of disgust facial expressions. Similarly,, Hennenlotter et al. (2004) showed decreased insulao disgust facial expressions in premanifest HD. Theseord with other research demonstrating the role of thegust processing using functional imaging (Calder et al.,ps et al., 1997;Wicker et al., 2003), intracerebral record--Salmon et al., 2003) and following focal brain damageranel, &Damasio, 2003; Calder, Keane, Cole, Campbell, &0); for a review see Calder, Lawrence, and Young (2001).rgest study of facial expression recognition in premani-ate, Johnson et al. (2007) investigated facial expressionin a group of 475 participants that tested positive

e but were yet to manifest the condition. The resultsaired recognition of negative facial expressions (anger,r, and sadness), but no evidence that disgust was dis-tely impaired. The premanifest group in this study waso four sub-groups on the basis of a standard motoramination (Unied Huntingtons Disease Rating Scale,burtz et al., 1996) relating to the clinicians condenceotor abnormalities were related to HD. Anger was theon impaired in all four subgroups, with the rst sub-imal evidenceofmotor impairments) showing impairedof anger only. The threeother subgroupswere impairedng anger, fear, and sadness, while the second and thirdwere impaired on disgust. A comparable analysis ofmes to categorise expressions showed slower RTs forll but the rst (least evidence of motor impairments)hereas subgroups 2 and 3 also showed reduced RTs to

essions.nce of a disproportionate impairment in recognisingJohnson et al.s (2007) study, the largest investiga-al expression recognition in premanifest HD to date,es that it is in no sense diagnostic of HD. Instead, likebehavioural decits associated with this complex neu-ic condition, emotion recognition decits may shown premanifest and manifest gene positive HD individ-rd & Snowden, 2002). However, from our review it ishere decits have been observed, these usually encom-han one emotion, particularly disgust, anger, and fear.disproportionate impairments have been reported foralso for anger, although the signicance of dispropor-

er impairments is generally not emphasised.nclusions are drawn from research that has focusedrecognition of emotion from faces rather than other

Fig. 1. Tcoded inand Rus

cues, atest, surelateswhethpopulations, h(2008)facial eand Haate disSprengdisgustion ofimpairpercepstratedRickarofmor& Dotyaccessgeneration ofstudy atogethet al.Similadid nonitionBachou

So fgust anis therfact thmodelin whithey ev(Fig. 1)

In tnitionevaluarcumplex model of emotion representation in which emotions areof their degree of arousal and unpleasantness;modied fromBullock

986).

nclusions are frequently based on the results of a singlehat it is unclear whether the variability among studiesifferences in stimulus materials, subject populations, orriable performance might also be observed in a singleacross different stimulus materials. There are excep-ver. Sprengelmeyer et al.s (1996) and Snowden et al.sstigations of manifest HD used at least two tests ofssion recognition, and both Sprengelmeyer et al. (1996)Stevenson, and Colheart (2007) found disproportion-impairments on tests of vocal emotion recognition.yer et al.s (2006) report of impaired recognition ofal expressions in premanifest HD also tested recogni-tion in the vocal modality but found no evidence ofcognitionof vocal expressions of any emotion. Impairedof disgust from olfactory cues has also been demon-yes et al., 2007); see also Mitchell, Heims, Neville, and005). However, these data need to be interpreted in lighteral olfactory impairments associatedwithHD (Moberg

A.J. Calder et al. / Neuropsychologia 48 (2010) 27192729 2721

whether decits on one test of facial expression recognition gen-eralized to another, and whether impairments in the facial domaingeneralized to the vocal modality and to semantic knowledge ofemotion. On the basis of previous research, we expected impairedrecognitionand fear, wIn additionimpairmenisons wereSprengelmenumber ofrecognizingquently affe

In a folloTheories offorms of disthat are evidistinctly hof social norcrimes). Thfor exampleaddressingobservationportionateanalysis of fLowery, antures are rerst subtypant tastes aThe secondsignalled byof social andis signalled

To addretypes of diRozin et al.series of shdisgust subselect whicmost approhealthy conaccuracy (Rrecognitionimpaired in

Previoustended to uthat includkled nose;facesmuscused in therecognitionneuroimagidisgust exp1997; Sprenthe neuraldisgust fearecent funccompared tcomprisingplaying mo2009). ResuexpressionsSince recogalso been linet al., 2007and possibl

Table 1Demographic data for participants with Huntingtons disease.

Huntingtons (n=21)

yearsince dR Esti/30a

a/28b

ia/20ll motndenonal aonal c

SE=MUHD

impat of dre apxpre

anc

dy 1

ethod

Partistudge=eir a

. Bacver

n, 19anc

n, & MuntinChounctsingvity cof spl ran

ign a

fam

lity to match pictures of unfamiliar faces was assessed withnton Test of Facial Recognition (Benton, Hamsher, Varney, &, 1983). On each trial of this test, the participant is shownt face and array of six faces. The task is to nd one or moreles of the target face amongst the array of six. Changes inrientation and lighting can occur between the target andaces.ognition of familiar faces was assessed with pictures of 30ties faces intermixed with 10 unfamiliar face foils (Calder et6; Young et al., 1995). The faces were presented individuallyeudo-random order. For each face, participants were askeder the person was familiar, and if so, to provide identifyingation (i.e., their occupation, nationality, lms they have beented with, etc.) and their name.of a number of emotions, particularly disgust, anger,ith more severe problems for disgust and/or anger., we were interested in whether a similar pattern oftswas foundacross differentmodalities. Group compar-conducted as in previous studies. However, followingyer et al. (2006), for each test we also calculated thepatients that demonstrated marked impairments ineach emotion to provide an estimate of the most fre-cted emotion in each test.w-up study, we focussed on disgust processing alone.disgust suggest a distinction between core, sensorygust related to reactions to unpleasant tastes or smellsdent across mammalian species, and a more complexuman form that incorporates a repugnance of violationsms or moral standards (e.g., sexual/physical abuse, waris latter form of disgust is closely aligned with anger ,we are both disgusted and angered by child abuse sodistinct forms of disgust is particularly pertinent to thethat disgust and anger are more likely to show dispro-

impairments in HD than other emotions. In a detailedacial expressionsofdisgust inhealthyvolunteers, Rozin,d Ebert (1994) showed that three different facial fea-liably associated with different disgust subtypes. Thee is associated primarily with the rejection of unpleas-nd is signalled by mouth gape and tongue protrusion.is associated with the rejection of unpleasant smells,nose wrinkle, while the third relates to the violationsmoral standards and interpersonal contamination and

by upper lip curl.ss HD participants recognition of these different sub-sgust facial expression, we used a test adapted from(1994) in which participants were presented with aort scenarios each depicting one of the three distincttypes. For each scenario, participants were required toh of the three disgust facial congurations provided thepriate facial reaction. Previous research has shown thattrols select the intended expression with above chanceozin et al., 1994). This enabled us to address whetherof a particular subtype of disgust expression might beHD.reports of facial expression recognition in HD have

se the Ekman and Friesen (1976) pictures of facial affecte disgust expressions with upper lip curl and wrin-two features that tend to co-occur as a result of theulature. These canonical disgust expressionshavebeenvast majority of studies investigating facial expressionin HD and other neurological conditions, as well as

ng studies addressing the neural correlates of viewingressions (Hennenlotter et al., 2004; Phillips et al., 1998,gelmeyer, Rausch, Eysel, & Przuntek, 1998). Although

mechanisms involved in processing each of the threetures discussed above have not been addressed, in ational magnetic resonance imaging (fMRI) study, wehe neural response to canonical disgust expressions,upper lip curl and nose wrinkle, with expressions dis-uth gape and tongue protrusion (von dem Hagen et al.,lts showed that only the upper lip curl/nose wrinkleengaged the anterior insula and frontal operculum.

nition of these canonical disgust expressions in HD hasked to insula function (Hennenlotter et al., 2004; Kipps), we expected that expressions with upper lip raisey the nose wrinkle expressions, would show the most

Age (inYearsNART-MMSEChoreDystonOveraIndepeFunctiFuncti

a MMb From

severevarianbe mogape eperform

2. Stu

2.1. M

2.1.1.The

mean atest; th

2.1.1.1revised(NelsoperformFolsteied H1996)Total Fprocessensitirangenorma

3. Des

3.1. Un

Abithe BeSpreena targeexamphead oarray f

Reccelebrial., 199in a pswhethinformassociaMean SD Range

s) 50.38 8.71 2865iagnosis 6.50 3.05 1.514

mated IQ 107.38 8.40 8712027.67 2.15 23307.57 5.47 020

b 1.38 2.31 08or score/124b 30.45 13.10 1450ce/100b 85.24 9.15 70100ssessment/50b 25.14 3.25 2031apacity/13b 9.45 2.25 612

ini mental state examination (Folstein et al., 1975).RS (Kieburtz et al., 1996).

irments. Moreover, the association of the upper lip curlisgust with anger suggested that impairments shouldparent for this variant of disgust. By contrast, mouthssions should be associated with comparatively sparede.

cipantsy included 21 patients with manifest HD (9 females;50.43, SD=8.70). Matched controls were used for eachge and IQ are reported in the results section below.

kground information. Intelligence was estimated withsion of the National Adult Reading Test (NART-R)91). Table 1 also summarises demographic details,e on the Mini Mental State Exam (MMSE) (Folstein,cHugh, 1975), and selected components from the Uni-

gtons Disease Rating Scale (UHDRS) (Kieburtz et al.,rea, Dystonia, Overallmotor score, Independence score,ional assessment and Functional capacity. Basic visualwas assessed using the VISTECH VCTS 6000 contrasthart. Two patients showed slightly low scores on mid-atial frequencies, otherwise performance was in thege.

nd procedure

iliar face matching and familiar face recognition


Fig. 2. The Emotion Hexagon test of facial-expression recognition. The six rows of this illustration contain morphed (blended) continua ranging between the following sixexpressionpairs. From top to bottom, the continua shown in each rowarehappinesssurprise (top row), surprisefear (second row), fearsadness (third row), sadnessdisgust(fourth row), disgustanger (fth row), angerhappiness (bottom row). Going from left to right, the columns show 90%, 70%, 50%, 30% and 10% morphs along each continuum.For example, from left to right, the top row of images contain the following percentages of the happy and surprised expressions: 90% happy10% surprise, and then 7030%,5050%, 3070% and 1090% of the same two expressions.


Table 2Performance of the Huntingtons patients and matched healthy controls on a test of unfamiliar face matching (Benton) and a test addressing recognition of famous celebritiesfaces, recalling their occupations and names, and correct rejection of unfamiliar faces. Percentage (and number) of patients showing severe impairments (z>2.33, p2.33 (p


details of the control groups for each test are provided at the endof each corresponding section. Controls were matched to HD par-ticipants for age and IQ, which did not signicantly differ.

Datawere available for all 21HDpatients for all tasks except theEmotion Hedata were c

4.1. Unfam

The HDis summarithat patienof unfamilimatched co2008; Snowal., 2003).

For recoicant reducidentifyingdid show m2.57, p


Table 5Performance of the Huntingtons patients and matched healthy controls on a testaddressing recognition of emotion from short verbal vignettes. Percentage (andnumber) of patients showing severe impairments (z>2.33, p


priate facial expression. From an initial study comprising multipledifferent facial expressions, a three-way choice procedure con-taining faces displaying one of the three disgust features (mouthgape/tongue protrusion, nose wrinkle, and upper lip curl) was pro-duced. Thefacial exprethat for thesion typeswHere we useaddress whately impai

As outlinupper lip cuthe resultsment, we pmore severMoreover, sgust expresfails to engtional integfacial expre2007) werelatively p

6. Method

6.1. Particip

The studticipated inIQ=106.95,(mean agefor years of

7. Design a

The expcomprisedphotographin a secondtrial a diffeprinted belthe participsion constitthe scenariprotrusionwith a worbottle thatfamous poldaughter.

There wios. Each scthe three fawith same euli were ide(ExperimenRozin et al.with scenartion. Exampexperimentof each of thandpictureto those incby calculatiexpressions

Table 6Performance of the Huntingtons patients (n=19) and matched healthy controls ona test addressing recognition of three types of disgust expression.

Scenario Face selected

rinkl

trols

gape

trols

lip

trols

cenaing th

ults

HDarisethatr eaccy: F.75;ronip 0.controrectedfrom cface lithe HDapproxing thaand exysed ththe Befamiliacriteriaas abowrinklrected

9. Dis

Ourfacialgust. Ina signidisgusfaces sgivenfacial ewe wosignallis of indisgustaminaNose Mouth gape Upper lip

e45% 31% 24%57% 21% 23%

28% 49% 24%21% 63% 17%

28% 35% 38%23% 17% 60%

rio. Data were then submitted to Chi-square analysese procedure used by Rozin et al. (1994).

and control participants performance for this test isd in Table 6. Consistent with Rozin et al. (1994) wecontrols selected the appropriate disgust facial expres-h of the three scenario types with well above chanceace 1 (nose wrinkle) 2 =40.82; Face 2 (mouth gape)Face 3 (upper lip curl) 2 =54.96; all analyses survivedcorrection for three comparisons (signicance thresh-.017). Next we compared the performance of the HDe performance of the controls again applying Bonfer-tion. Results showed a borderline but non-signicantetween HD and controls for nose wrinkle (face 1) and(face2) (2 =6.64 and2 =7.49, respectively; corrected

and a highly signicant discrepancy between HD andformance for upper lip curl (face 3), 2 =21.95, cor-.001. Thus, theHDpatients show the largest discrepancyls for scenarios relating to face 3 (upper lip curl), themore to moral disgust. In fact, as shown in Table 6,

ients selected each of the three expression types withely equal frequency for the face 3 scenarios, illustrat-y did not show the association between upper lip curled disgust shown by the controls. Finally, we reanal-ta excluding the three patients who were impaired onand one or more aspects of recognising famous faces asntifying occupations, and identifying names (the same

d in Study 1) and found that the same signicant effectshe results were consistent with the rst analysis: nose=5.54; mouth gape/tongue protrusion, 2 =3.15 (cor-0.1), and upper lip curl, 2 =19.66 (corrected p


is closely associated, or often accompanied by anger. Our ndingsalso accord with recent functional imaging research showing thatthe insula cortex is responsive to disgust expressions comprisingupper lip curl, but not disgust expressions comprising mouth gapeand tongue

10. Genera

Our studtion from fHD. In addiof impairedmaterial. Aof facial antional vignethe differenshowed a gfor other emof differentthat HD indisgust fromforms of digape/tonguthat did notrast, they supper-lip cgust that inGiven the remore closelTo this exteof anger-rel

As outlinfacial expredisproportigust (Montal., 2003). Avocal and odisgusting p(Hayes et alfound no eval., 2008; Mis of note thnition of emcues, Snowdemotions, wLikewise, Hment in recet al. (2008emotions (tThus, of theHD to date,disgust stim(Hayes et a1996; Wantional studi(de Gelder e

In the stion in preHennenlottMilders etgust impairHennenlottremaining sthat anger wifest patien

ecognd verance.

as Kiin thummve shhowhersctio

hat aplexcitsns (svocas relceilins ademogreggestingregootionin in001;000;monaroutiona, follio, 19ula (C0; Cdimemenet alctive summary of the relationship or confusability of differ-otions and Fig. 3 demonstrates that the impairment in ourticipants ismaximal for anger and least evident for emotionsemost dissimilar to anger. Similarly, in Study2, patientswithwed an impairment for the disgust subtype most associatednger.emains to be explained, however, why some studies havemore severe impairments for disgust and others for anger.terpretation is that essentially the same decit is present ints with HD. This decit affects the interpretation of signals ofisapproval, such as disgust and anger, but the relative sever-mpairments for these emotions derives from other factors,least of which may reect the variants of disgust or anger

sised in different tests of emotion recognition. As an expla-protrusion (von dem Hagen et al., 2009).

l discussion

y found marked impairments in recognition of emo-acial and vocal expressions in patients with manifesttion, the emotional vignettes task provided evidenceconceptual understanding of emotion from verbal

nger, fear, and disgust, were impaired across all testsd vocal expression recognition, whereas for the emo-ttes task the impairmentwas restricted to anger. Acrosst modalities, we found that the participants with HDreater number of severe impairments for anger thanotions. In a second study focussing on the recognitionfacial action units associated with disgust, we found

dividuals showed comparatively good recognition offacial congurations associated with core, sensory

sgust unpleasant tastes or oral sensations (mouthe protrusion) and unpleasant smells (nose wrinkle) t signicantly differ from control performance. In con-howed severely impaired recognition of disgust fromurl faces associated with the expanded form of dis-cludes reactions to violations of social andmoral norms.sults of Study 1, it is of interest that expanded disgust isy alignedwith anger than the other disgust expressions.nt, both the rst and follow-up studies show evidenceated impairments.ed in Section 1, a number of previous investigations ofssion recognition in manifest HD patients have foundonate impairments in recognising facial signals of dis-agne et al., 2006; Sprengelmeyer et al., 1996; Wang etfourth study showed a similar disgust impairment forlfactory cues, together with impaired classication ofictures and declarative knowledge of disgust elicitors., 2007). In contrast, other studies of manifest HD haveidence of disproportionate disgust decits (Henley etilders et al., 2003; Snowden et al., 2008). However, itat using a similar format to our own addressing recog-otion from short verbal vignettes and facial and vocalen et al. (2008) found impaired recognition of negativeith anger showing the most consistent impairment.

enley et al. (2008) also found a disproportionate impair-ognising anger from facial expressions, and de Gelder) reported impaired recognition of anger, but not otherhough they did not test disgust) from animated bodies.nine investigations of emotion recognition in manifestincluding our own, four out of the eight that includeduli found a disproportionate impairment for disgustl., 2007; Montagne et al., 2006; Sprengelmeyer et al.,g et al., 2003), whereas our own study and three addi-es have found disproportionate impairments for angert al., 2008; Henley et al., 2008; Snowden et al., 2008).even studies investigating facial expression recogni-manifest HD (Gray et al., 1997; Henley et al., 2008;er et al., 2004; Johnson et al., 2007; Kipps et al., 2007;al., 2003; Sprengelmeyer et al., 2006), selective dis-ments have been reported in three (Gray et al., 1997;er et al., 2004; Sprengelmeyer et al., 2006). Of thetudies, it is of interest that Johnson et al. (2007) foundas the only emotion that was impaired in all preman-

ts, regardless of their probability of having early HD,

Fig. 3. Rvocal, anperform

whereanger,

In sdate hasome sand otintrodutions tCircumthe deemotiofacial,z scoredue toemotio(Fig. 1)gets prThis suaccounthereafor eming braet al., 2et al., 2most acodingproporas fearDamasthe insal., 200eitherimpairCalderan effeent emHDparthat arHD showith a

It rshownOne inpatiensocial dity of inot theemphaition of surprise, fear, anger, disgust, and sad emotions from the facial,bal tasks expressed as mean z scores calculated relative to control

pps et al. (2007) reported a borderline impairment fore context of intact recognition of other emotions.ary, investigations of emotion recognition in HD toown evidence of impaired recognition of emotionwithing disproportionately severe impairments for disgustshowing more marked impairments for anger. In then, we noted that anger and disgust are confusable emo-re positioned next to one another in Russells (1980)model of emotion. Fig. 3 summarises the magnitude ofshown by the HD group from our rst study for the veurprise, fear, anger, disgust, and sadness) tested in thel, and verbal tasks. The decits are expressed as meanative to control performance and happiness is omittedng effects in the controls. It is striking that ordering theccording to their arrangement in the Circumplex modelonstrates that the decit seems to centre on anger andssively less severe with increasing distance from anger.ts that the Circumplex model may have some value infor thepatternof emotion impairments inHD.However,od reasonswhy thismodel cannotprovidea full accountrecognition and patterns of impairments found follow-

jury or in neuropsychiatric disorders such as HD (CalderCalder, Keane, Cole, et al., 2000; Calder, Keane, Manes,Calder, Rowland, et al., 2000; Young et al., 1997). Fore-g these is that a system based on just two dimensionssal and pleasantness cannot explain selective or dis-te impairments in recognising distinct emotions, such

owing amygdala damage (Adolphs, Tranel, Damasio, &94; Calder et al., 1996), or disgust following damage toalder, Keane, Cole, et al., 2000; Calder, Keane,Manes, et

alder, Rowland, et al., 2000). This is because damage tonsion (arousal or valence) would result in more generalts affecting more than one emotion; for a discussion see. (2001). However, the Circumplex model does provide


nationofwhyonly some studies of emotion recognition inHDshowevidence of disgust impairments, Snowden et al. (2008) suggestedthat differences in the precise denitions of emotion labels used indifferent languages may be important. Five studies that show noevidence ofown) wereet al., 2008et al., 2008ing disgustfrom Germaal., 2006, 1out that therefers to a mcarries bothconductedof the woris related cthat of disguthan Germagust impairin China, MGray et al.sthe UK, andemotion recSo it seemsthe differenin future stu

It is alsomay have dto differingrecent invebasedmorpthat their dof the anterlished role2007; Caldeal., 2000; CaKeysers, & Ral., 1997;Wtion impairatrophy inHof facial andtral putamepremanifesrelative protral putameimpairmen

Unfortunmeans thatis also worinvolved instages of thbetween thtion of angeby the exteof the diseationship becould intera

It is alsobeen observsuch as coexplosive dsociopathytherefore otability are& Snowden

Hence, it is possible that anger and disgust impairments in HD aremodulated by the presence of aggressive/irritable behaviour, andit may be fruitful to explore this relationship in future research.

In line with the idea that impairments in disgust and angeritiond thasignady i

r eaccit imated inincesionntri

l expg thgageed bet algests thles oe andcal dtasteen topremn ety in pgusta thala funt faetimotheummangebeingshowor

ed diwo eoss the ininHDtosoal stat wncesnt lanterc8), ah. Fmen2002ouren lenstit

wled

wouts anseardisproportionate disgust impairments (including ourconducted in native English speaking groups (Henley; Johnson et al., 2007; Milders et al., 2003; Snowden), whereas a signicant proportion of the work show-impairments in premanifest and manifest HD has comen groups (Hennenlotter et al., 2004; Sprengelmeyer et

996, 1997). In particular, Snowden et al. (2008) pointGerman term for disgust used in these studies, Ekel,ore visceral disgust reaction, whereas the English termvisceral and moral connotations. Moreover, a study

in North America showed that the lay understandingd disgust corresponds more to the moral form andlosely, if not more so, to the meaning of anger as tost (Nabi, 2002). However, studies from countries otherny have also found evidence of disproportionate dis-ments, including Wang et al.s (2003) study conductedontagne et al.s (2006) investigation in the Netherlands,(1997) investigation of premanifest HD participants inHayes et al.s (2007) Australian study which addressedognition from modalities other than facial expressions.unlikely that different meanings alone could explaint ndings, but this point will need to be borne in minddies addressing emotional processing.worth considering that disgust and anger impairmentsifferent neurological bases that could be compromiseddegrees in cases of symptomatic HD. For example, a

stigation of premanifest HD participants using a voxel-hometry (VBM)analysisof structural braindata showedisgust recognition was related to grey matter volumeior insula (Kipps et al., 2007), a region with an estab-in this emotion (Adolphs et al., 2003; Calder et al.,r, Keane, Cole, et al., 2000; Calder, Keane, Manes, etlder, Rowland, et al., 2000; Calder et al., 2001; Gallese,izzolatti, 2004; Krolak-Salmon et al., 2003; Phillips eticker et al., 2003). Thus, the presence of disgust recogni-ments may be governed by the extent of anterior insulaDpatients. Similarly, there is evidence that recognitionvocal signals of anger is affected by damage to the ven-n (Calder et al., 2004), a region that is also reduced int HD (Kipps et al., 2005; Thieben et al., 2002). Hence, theportion of damage to areas such as the insula and ven-n might determine whether the emotion recognition

t in HD is more severe for anger or disgust.ately, the lack of structural MRI scans in our studywe are unable to address this question. However, it

th considering that HD affects areas of frontal cortexprocessing multiple emotions, even in the premanifeste disease (Thieben et al., 2002). Thus, any relationshipe recognition of disgust and insula volume or recogni-r and putamenal volume may be affected (or masked)nt of frontal atrophy, particularly in the manifest formse as frontal damage increases. In otherwords, any rela-tween emotion recognition and the insula or striatumct with the effects of atrophy to other brain areas.worth noting that disgust and anger impairments haveed in disorders of aggression and anti-social behaviour,nduct disorder (Fairchild et al., 2009), intermittentisorder (Best, Williams, & Coccaro, 2002), or acquiredfollowing brain injury (Blair & Cippolotti, 2000). It isf particular note that aggressive outbursts and irri-a common behavioural manifestation of HD (Craufurd, 2002; Vassos, Panas, Kladi, & Vassilopoulos, 2007).

recognshoweanger,this stusion fothe deverbalimpairever, sexpresmay colip curshowinture ensignallHagenhas sugengageexampwrinklcanonithe dis

Takin theThiebeatrophical disthe ideto insudiffereis somand in

In snisingangerstudiesrecentreportthese ters acrdate. Tmentslinkedof mortion thdifferediffereshow ial., 200researcimpairet al.,behavibetwemay co

Ackno

WepatienThe Reare associated with HD, it is of interest that Study 2t the disgust subtype that is most often associated withlled by upper lip curl, was particularly impaired. Since

nvolved selecting the most appropriate disgust expres-h verbal emotional scenario, it is difcult to tellwhethers caused by impaired conceptual understanding of theerial associated with the relevant disgust subtype orterpretation of its associated facial expression. How-Study 1 showed evidence of impairments for the facialand emotional vignettes tasks, it is possible that bothbute. As discussed, marked impairments for the upperressions accordswith our recent neuroimaging researchat canonical disgust expressions comprising this fea-the anterior insula, whereas the distaste expressions

y mouth gape and tongue protrusion do not (von dem., 2009).We recognise that previous neuroimagingworked that viewing facial reactions tounpleasant tastes alsoe insula (Jabbi, Swart, & Keysers, 2007). However, thef disgust expressions used by Jabbi et al. comprised noseupper lip curl, meaning that they were similar to the

isgust expressions used by von demHagen et al, and not(mouth gape/tongue protrusion) expressions.gether with the reports of insula atrophy in HD, evenanifest stages (Kassubek et al., 2004; Kipps et al., 2005;al., 2002), and work showing that the extent of insularemanifest HD is correlated with recognition of canon-expressions (Kipps et al., 2007), our results converge ont HD affects a particular form of disgust that is relatednction and closely aligned with anger. Moreover, thectors we have discussed may explain why the decites expressed as a disproportionate disgust impairmentr studies as a more severe impairment for anger.ary, our study shows evidence of impairments in recog-r, fear and disgust in patients with manifest HD, withthe most severely affected. A review of other relevant

wed that similar ndings have been reported in otherk. In addition, a sizeable number of studies have alsosproportionate impairments in recognising disgust, andmotions showmoremarked impairments than any oth-he literature addressing emotion processing in HD tocreased incidence of severe disgust and anger impair-may pertain to the fact that a particular formof disgust

cial disapproval that incorporates reactions toviolationsandards is closely aligned with anger; an interpreta-as supported by the results of Study 2. However, subtlein the denition of emotion labels used for disgust innguages may also help explain why these two emotionshangeable disproportionate impairments (Snowden etnd this should be taken into consideration in futureinally, we have emphasised that anger and disgustts are also observed in disorders of aggression (Best; Fairchild et al., 2009). The presence of aggressivein HD is notable to this extent and the relationshipvels of aggression and anger/disgust impairments in HDute an interesting avenue for future research.

gements

ld like to extend our sincere thanks to the Huntingtonsd their families, for giving us their time and assistance.ch was funded by the Medical Research Council, UK


(U.1055.02.001.00001.01 to AJC). ADL acknowledges support fromthe Wales Institute of Cognitive Neuroscience and Parkinsons UK;RAB acknowledges support from an NIHR Biomedical ResearchCentre grant to Addenbrookes Hospital and the University of Cam-bridge. Thanused in Stud

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The relation between anger and different forms of disgust: Implications for emotion recognition impairments in Huntington'...IntroductionStudy 1MethodParticipantsBackground information

Design and procedureUnfamiliar face matching and familiar face recognitionFacial expression recognitionEkman 60Emotion Hexagon

Vocal expression recognitionNon-verbal emotional sounds

Conceptual understanding of emotionEmotional vignettes

Results and discussionUnfamiliar face matching and familiar face recognitionEmotion recognitionFacial expression recognitionEkman 60Emotion Hexagon

Vocal expression recognitionNon-verbal emotional sounds

Conceptual understanding of emotionEmotional vignettes

Study 2MethodParticipants

Design and procedureResultsDiscussionGeneral discussionAcknowledgementsReferences

Documents

18 Saenz Leandro - Calder