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Attentional bias to negative emotion as a function of approach and withdrawal angerstyles:An ERP investigationJennifer L.Stewarta,b,Rebecca Levin Siltonb,c,Sarah M.Sassb,Joscelyn E.Fisherb,d,J.Christopher Edgarb,e,Wendy Hellerb,f,Gregory A.Millerb,faDepartment of Psychology,University of Arizona,Tucson,AZ,USAbDepartment of Psychology,University of Illinois at Urbana-Champaign,Champaign,IL,USAcDepartment of Psychiatry,Seattle Childrens Hospital,Seattle,WA,USAdDepartment of Psychiatry,University of Maryland School of Medicine,Bethesda,MD,USAeDepartment of Radiology,Childrens Hospital of Philadelphia,Philadelphia,PA,USAfBeckman Institute Biomedical Imaging Center,University of Illinois at Urbana-Champaign,Champaign,IL,USAa b s t r a c ta r t i c l ei n f oArticle history:Received 14 August 2009Received in revised form 17 January 2010Accepted 19 January 2010Available online 25 January 2010Keywords:AngerEmotionMotivationCognitive resourcesEvent-related potentialsAlthough models of emotion have focused on the relationship between anger and approach motivationassociated with aggression,anger is also related to withdrawal motivation.Anger-out and anger-in styles areassociated with psychopathology and may disrupt the control of attention within the context of negativelyvalenced information.The present study used event-related brain potentials(ERPs)to examine whetheranger styles uniquely predict attentional bias to negative stimuli during an emotionword Stroop task.Highanger-out predicted larger N200,P300,and N400 to negative words,suggesting that aggressive individualsexert more effort to override attention to negative information.In contrast,high anger-in predicted smallerN400 amplitude to negative words,indicating that negative information may be readily available(primed)for anger suppressors,requiring fewer resources.Individuals with an anger-out style might benefit frombeing directed away from provocative stimuli that might otherwise consume their attention and foster overtaggression.Findings indicating that anger-out and anger-in were associated with divergent patterns of brainactivity provide support for distinguishing approach-and withdrawal-related anger styles.2010 Elsevier B.V.All rights reserved.1.IntroductionResearchers have postulated approach-and withdrawal-relatedmotivational systems that are implemented in several brain regionsand that play a crucial role in the experience and expression ofemotion.Anger,a feeling evoked when individuals believe that theyor others are treated badly or unfairly(Averill,2001),involvesapproach and/or withdrawal behavior depending on context(e.g.,Berkowitz,1990;Watson,2009;though see Carver and Harmon-Jones,2009).Spielberger(1988,1999)developed the State-TraitAnger Expression Inventory(STAXI),which conceptualizes angerexpression styles that occur in connection with angry feelings.TheSTAXI anger-out scale reflects aggression,defined as the expression ofangry verbal or motor behavior directed toward people or objects,whereas the STAXI anger-in scale is conceptualized as measuringsuppression or inhibition of outward signs of anger and/or withdraw-ing from an anger-inducing situation.Approach(anger-out)and withdrawal(anger-in)anger stylesmay disrupt the control of attention in the context of negativelyvalenced information,interfering with successful emotion regulation.Several behavioral studies have indicated that angry individualsdisplay an attentional bias toward negatively valenced stimuli(e.g.,Cohen et al.,1998;Eckhardt and Cohen,1997;Kirsch et al.,2005;Smith and Waterman,2003,2004;van Honk et al.,2001)that couldunderlie the potential for angry individuals to perceive ambiguoussituations as hostile and/or threatening(e.g.,Hazebrook et al.,2001;Wenzel and Lystad,2005).Furthermore,approach and withdrawalanger styles may differ in the timing and activation of attentional biasto negative stimuli.Unlike behavioral measures such as reaction time(RT),event-related brain potentials(ERPs)offer multiple,millisecond measure-ments of attentional processes.However,little research is available onERP effects associated with an anger-out style(Patrick and Verona,2007),and none has specifically examined ERPs associated with anInternational Journal of Psychophysiology 76(2010)918 This study was submitted in partial fulfillment of dissertation requirements at theUniversity of Illinois at Urbana-Champaign for Jennifer L.Stewart.This research wassupported by the National Institute of Drug Abuse(R21 DA14111),the NationalInstitute of Mental Health(P50 MH079485,R01 MH61358,T32 MH19554),and theUniversity of Illinois Beckman Institute,Department of Psychology,and IntercampusResearch Initiative in Biotechnology.Corresponding author.Department of Psychology,University of Arizona,1503 EastUniversity Boulevard,Tucson,AZ 85721,USA.Tel.:+1 520 626 5401;fax:+1 757 2576344.E-mail address:jlstewaremail.arizona.edu(J.L.Stewart).0167-8760/$see front matter 2010 Elsevier B.V.All rights reserved.doi:10.1016/j.ijpsycho.2010.01.008Contents lists available at ScienceDirectInternational Journal of Psychophysiologyjournal homepage: style.ERP studies of aggression have primarily used oddballtasks consisting of either auditory or visual stimuli and have focusedon the parietally distributed P300 component,typically in patient orinmate populations(e.g.,Barratt et al.,1997;Bernat et al.,2007;Harmon-Jones et al.,1997;Stanford et al.,2003),although college andcommunity populations have also been examined(e.g.,Gerstle et al.,1998;Mathias and Stanford,1999;Surguy and Bond,2006).P300,apositive deflection typically occurring 300 to 600 ms post-stimulus-onset,is thought to reflect stimulus evaluation,attention allocation,and context updating(e.g.,Coles et al.,2000;Donchin and Coles,1988).Results of these P300 studies suggest a link between impulsiveaggression and reductions in parietal P300 amplitude(Barratt et al.,1997;Harmon-Jones et al.,1997).Most ERP studies of aggression have employed non-emotionalwords or sounds as oddball stimuli,so it is unclear whether theassociation between reduced P300 amplitude and aggression gen-eralizes to or differs from anger-or aggression-related stimuli.Thesingle ERP study incorporating negatively valenced stimuli found thatmale community members high in aggression displayed reducedfrontal P3a in response to non-target aggressive words in a visualoddball task,but these P3a reductions were in the absence of parietalP300 decrements in response to targetneutral food-related words(Surguy and Bond,2006).Whereas P300 is thought to reflect evaluation of stimulussignificance,N100(a negative deflection occurring around or shortlyafter 100 ms)and P200(a positive deflection occurringabout 200 ms)are components with frontocentral scalp distributions thought toreflect attention to stimuli during relatively early,perceptual stages ofprocessing(e.g.,Hillyard et al.,1998;Junghfer et al.,2001;Ntnenet al.,1982).In contrast to earlier components like the N100 andP200,the visual N200 is a negative-going ERP component occurring200300 ms post-stimulus,with a right-lateralized frontocentralscalp distribution localized to a right prefrontal source(Strik et al.,1998),thought to reflect response inhibition and/or conflict moni-toring(e.g.,van Veen and Carter,2002).N400 indexes elaborativestimulus processing in that it is modulated by semantic meaning.Larger N400 amplitude is associated with improbable words,whereassmaller N400 amplitude is associated with facilitated processing(e.g.,for words of higher lexical frequency or words primed within aparticular sentence context;Kutas and Hillyard,1980;van Petten andKutas,1990).Although N400 is reduced for emotional stimuli that areprimed(Schirmer et al.,2002,2005),it is also attenuated foremotional stimuli compared to neutral stimuli in the absence ofexplicit priming(Kanske and Kotz,2007).If amplitudes of earliercomponents such as N100 or P200 are reduced in size,conclusionsabout aggression and its relationship to attention cannot be limited tolater,“top-down”processes involving attentional control such asN200,P300,or N400.ERP studies of aggression have not typicallyanalyzed components other than P300,although one study usingneutral stimuli found no relationship between aggression and N100,P200,or N200 amplitude(Barratt et al.,1997).The present study examined whether approach and withdrawalanger expression styles were differentially associated with attentionalbias to negative words in an emotionword Stroop task above andbeyond measures of negative affect that are highly comorbid withanger expression such as depression,anxiety,and trait anger(e.g.,Deffenbacher et al.,1996).Neural mechanisms involved in attentionto emotional stimuli were measured using N100,P200,N200,P300,and N400 amplitude scores.The specificity of any such effects tonegative stimuli was evaluated by inclusion of positive and neutralstimuli.Differential predictions were made regarding ERP amplitude tonegative stimuli in anger styles,despite lack of guidance from theliterature.It was hypothesized that higher anger-in scores wouldpredict larger N200,P300,and N400 amplitude in response tonegative words,as more resources may be needed for high anger-inindividuals to suppress outward angry responses.In contrast,it waspredicted that anger-out would be linked to reduced N200,P300,andN400 amplitudes to negative stimuli based on prior P300 researchutilizing non-emotional stimuli with aggressive individuals.It waspredicted that the two anger styles would diverge only whenexecutive control was needed(reflected in N200,P300,and N400amplitude)to override attention to negative valence in order to selectthe correct color response.It was likely that differences in brain activation as a function ofanger style would occur without behavioral differences in RT or errorrates(e.g.,longer RT and more errors for negative stimuli than forpositive or neutral stimuli),since in nonclinical samples,includingsamples indexing traits such as anxiety,RT impairment fromemotional content is attenuated in the emotionword Stroop task(e.g.,Franken et al.,2009;Thomas et al.,2007).Thus,in the presentstudy the focus was on ERP indices of attentional bias to emotionalstimuli.2.Method2.1.ParticipantsParticipants were 102 paid undergraduates(54 female,81%Cauca-sian,mean age=19.02,SD=1.74)recruited via group questionnairesessions in which measures of anger,anxiety,and depression wereadministered.Participants completed the Anger Expression-In,AngerExpression-Out,and Trait Anger scales from the State-Trait AngerExpression Inventory 2(STAXI-2;Spielberger,1999).STAXI-2Anger Expression-In and Anger Expression-Out are 8-item scales onwhich participants rate how they generally react or behave when angryor furious(1=almost never,2=sometimes,3=often,4=almostalways).Examples of Anger Expression-In items are“I boil inside butdont show it”and“I withdraw from people.”Examples of AngerExpression-Out items are“I strike out at whatever infuriates me”and“Ido things like slam doors.”STAXI-2 Trait Anger is a 10-item scale thatmeasures individual differences in the predisposition to express angerand react angrily to situations involving frustration or negativeevaluation.In addition to the Trait Anger scale,participants wereadministered other measures of negative affect to assess depressionand types of anxiety that may co-occur with anger styles:the Penn StateWorry Questionnaire(PSWQ;Meyer et al.,1990)to assess anxiousapprehension,or worry,and the Anxious Arousal(AA)and AnhedonicDepression(AD)scalesoftheMoodandAnxietySymptomQuestionnaire(MASQ;Watson et al.,1995)to assess anxious arousal,or somaticanxiety,andanhedonicdepression.Asubscaleof8itemsfromtheMASQ-AD was used that identifies depressed mood and loss of interest distinctfrom other items reflecting low positive affect(Nitschke et al.,2001).Means and standard deviations for STAXI-2,PSWQ,MASQ-AA,and 8-item MASQ-AD scales are provided in Table 1,and correlations betweenscales are presented in Table 2.1Results indicate that,although higheranger-in and anger-out scores were both associated with higher traitanger scores,anger-in(but not anger-out)was positively linked todepression and types of anxiety,with anger-in possessing a significantlyhigher correlation with anxious apprehension than anger-out(p0.01).1All participants in this sample were recruited for a larger study on the basis ofhigh(above the 80th percentile)and low(below the 50th percentile)scores on PSWQ,MASQ-AA,and8-itemMASQ-ADscalesgatheredduringgrouptestingsessions(PSWQ:72low-scoring subjects,30 high;MASQ-AA:74 low,28 high;8-item MASQ-AD:72 low,30high).The STAXI-2,PSWQ,and MASQquestionnaires werereadministeredtoparticipantsduring an individual laboratory tour,and these scores were used in the present study.Subjectsselectedwiththesecriteriarepresentmostoftherangeofthescales(allbutabout1SD),sothisisnotatraditionalextreme-groupsstrategy.Furthermore,someregressiontothemeanoccurredfromthetimeofthemasstestingsessiontothelabtoursession;Table1indicates that 2432%of the sample moved into the 50th to the 80th percentile range onthe PSWQ and MASQ scales,demonstrating a relatively normal distribution of scores onthese measures.10J.L.Stewart et al./International Journal of Psychophysiology 76(2010)918All participants provided informed consent,were right-handed withaverage Edinburgh Handedness(Oldfield,1971)laterality quotientM=78.96(SD=17.52),native speakers of English with self-reportednormal color vision who were free of traumatic brain injury and othermedicalconditionsknowntoaffectcentralnervoussystemfunction(e.g.,epilepsy).This study was approved by the university IRB beforeparticipants were recruited,and therefore this research has beenperformed in accordance with the ethical standards of the 1964Declaration of Helsinki.2.2.Stimuli and experimental designParticipants2completed a colorword Stroop task and an emotionword Stroop task.Both tasks were administered during an EEG sessionand again during an fMRI session.The order of presentation of the twoStroop tasks within a session was counterbalanced across participants,as was the order of the EEG and fMRI sessions,with a diagnosticinterview session in-between(49 participants were assigned EEGsessions first,whereas the remaining 53 were assigned fMRI sessionsfirst).Data from the emotionword Stroop task completed during theEEG session are reported in the present study.3Wordpresentation and response recordingwere controlled bySTIMsoftware(James Long Company,Caroga Lake,NY).Several pilot studiesfor this project as well as published work show that a blocked design ismore effective in eliciting emotionword Stroop interference than is anintermixed design(e.g.,Compton et al.,2003;Dalgleish,1995).Theemotionword Stroop task consisted of blocks of positive or negativeemotion words alternating with blocks of neutral words.Participantsreceived 256 trials in 16 blocks(4 positive,8 neutral,and 4 negative)of16 trials.A trial began with the p
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