While bottom-up processing of emotional stimuli is adaptivewhentheyarerelevanttoourwell-being, itisequally adaptivetoignorethesestimuliandstaytask-focusedwhenthey posenodanger.Hence,adap
Trang 1Contents lists available atScienceDirect
Biological Psychology
j o u r n a l h o m e p a g e :w w w e l s e v i e r c o m / l o c a t e / b i o p s y c h o
Top-down and bottom-up factors in threat-related perception and
attention in anxiety
Tamara J Sussman, Jingwen Jin, Aprajita Mohanty∗
Department of Psychology, Stony Brook University, United States
a r t i c l e i n f o
Article history:
Received 14 September 2015
Received in revised form 10 August 2016
Accepted 17 August 2016
Available online xxx
Keywords:
Top-down
Endogenous
Threat perception
Prestimulus processes
Attention
Amygdala
Anxiety
Sensory cortex
Prefrontal cortex
Perceptual bias
Attentional bias
a b s t r a c t
Anxietyischaracterizedbytheanticipationofaversivefutureevents.Theimportanceofprestimulus anticipatoryfactors,suchasgoalsandexpectations,iswell-establishedinbothvisualperceptionand attention.Nevertheless,theprioritizedperceptionofthreateningstimuliinanxietyhasbeenattributed
totheautomaticprocessingofthesestimuliandtheroleofprestimulusfactorshasbeenneglected.The presentreviewwillfocusontheroleoftop-downprocessesthatoccurbeforestimulusonsetinthe perceptualandattentionalprioritizationofthreateningstimuliinanxiety.Wewillreviewboththe cog-nitiveandneuroscienceliterature,showinghowtop-downfactors,andinteractionsbetweentop-down andbottom-upfactorsmaycontributetobiasedperceptionofthreateningstimuliinnormalfunction andanxiety.Theshiftinfocusfromstimulus-driventoendogenousfactorsandinteractionsbetween top-downandbottom-upfactorsintheprioritizationofthreat-relatedstimulirepresentsanimportant conceptualadvance.Inaddition,itmayyieldimportantcluesintothedevelopmentandmaintenanceof anxiety,aswellasinformnoveltreatmentsforanxiety
©2016ElsevierB.V.Allrightsreserved
Emotionalstimuli requirerapid adaptive responses, suchas
avoidanceofthreatorapproachtowardsarewardingstimulus.To
allowfor theseswiftbehaviouralresponses,ourperceptualand
attentionalsystemprioritizesemotionalstimulioverstimulithat
arerelatively unemotionalin nature.Spiders,snakesand angry
facesarehypothesizedtobelongtoaspecialclassofstimulithat
areperceptuallyprioritizedduetotheirimportanceforsurvival
(Brosch,Pourtois,&Sander,2010;New,Cosmides,&Tooby,2007;
Seligman,1971).Empiricalresearchsupportingthisviewshows
that spiders and snakesare detectedmore rapidlythan
mush-roomsandflowers(Ohman,Flykt,&Esteves,2001)and.angryfaces
aredetectedfasterthan neutralfaces(Hansen&Hansen,1988;
Horstmann,2007).Saccadiceyemovementsorientmorequicklyto
imagesofthreateningcomparedtoneutralfacesandbodypostures
(Bannerman, Milders,de Gelder, & Sahraie, 2009) Threatening
∗ Corresponding author at: Department of Psychology, Stony Brook University,
Stony Brook, NY 11794, United States.
E-mail address: aprajita.mohanty@stonybrook.edu (A Mohanty).
stimulishownrapidlyinastreamofimagesareidentifiedmore accuratelythanneutralstimuli(Anderson,2005).Whilepositive stimulimayalsobeassociatedwithsimilarperceptualbenefits,the effectstendtobesmallerthanthoseelicitedbythreateningstimuli (Carretie,Mercado,Tapia,&Hinojosa,2001;Dijksterhuis&Aarts,
2003;Smith,Cacioppo,Larsen,&Chartrand,2003;Stefanics,Csukly, Komlosi, Czobor, &Czigler, 2012; Sussman,Weinberg, Szekely, Hajcak,&Mohanty,2016)
The facilitated perception of threatening stimuli has been attributedtobottom-upprocessingdrivenbythephysical charac-teristicsorevolutionarysignificanceofthesestimuli(Bannerman
etal.,2009;Ohmanetal.,2001).Inlinewiththisview,research
inaffective neurosciencehascenteredonexaminingtheneural pathwaysthatpromote‘automatic’perceptionofemotional stim-uli(Fox,2002;Mendez-Bertoloetal.,2016;Vuilleumier&Pourtois,
2007).Itishypothesizedthatthreateningstimuliareprioritized duetoaprocessingbias(Bar-Haim,Lamy,Pergamin, Bakermans-Kranenburg,&van,2007; Cisler,Bacon,&Williams,2009).This processingbiasisnotmeasureddirectly,andinsteadisinferred fromaccuracyandreactiontimedifferencesbetweenthe detec-tionofthreateningcomparedtoneutralstimuli.Dependingonthe designofthetask,thethreatbiasishypothesizedtofacilitate detec-http://dx.doi.org/10.1016/j.biopsycho.2016.08.006
0301-0511/© 2016 Elsevier B.V All rights reserved.
Trang 2orimpedeperformancewhenthreateningstimulidistractfromthe
taskathand(Mathews&MacLeod,1994;Ohmanetal.,2001).Here,
weexplorethepossibilitythatinadditiontoprocessingbiasesthat
occurcoincidentwithstimuluspresentation,prioritized
percep-tionofthreateningstimuliinnormalfunctionandanxietymaybe
attributedtoprestimulusbiases
Theideathat prestimulusbiases impactthreat-perceptionis
consistentwithresearchindicatingthattheprocessofperception
startspriortoanencounterwithastimulus,and withresearch
demonstratingthatperceptionisguidedbytop-downfactorssuch
asgoalsandexpectations(Bacon&Egeth,1994;Itti&Koch,2001)
Forexample,bothimplicitandexplicitprestimuluscuesimprove
target perception (Chen & Zelinsky, 2006; Wolfe, Butcher, Lee,
&Hyle, 2003) Similarly, in day-to-day life, we often use both
implicitandexplicitemotionalinformationtoguideour
percep-tion,forexample, whilescanningfor spidersin anuninhabited
roomfilled withcobwebs Theseanticipatorysearch behaviors,
aimedatrapidlydetectingsourcesofpotentialrewardorthreat,are
deployedinawiderangeofsituationsfromdrivingonahighwayto
navigatingsocialgatherings.Prestimulusbiasesmaybeof
partic-ularimportanceinanxiety,asdispositionalanxietyisassociated
withoverestimation of the likelihood and cost of future
nega-tiveevents(Aue&Okon-Singer,2015;Grupe&Nitschke,2013)
Theimportanceoftop-downprocessesinanxietyhasalsobeen
demonstratedbystudiesshowingthatthreat-relatedcuesimpact
subsequentperceptiondifferentlydependingontypeofanxiety
(Sussman,Szekelyetal.,2016)
In the present review we first discuss the current
affec-tiveneuroscienceliteratureonexogenous,‘bottom-up’factorsin
understandingperceptualandattentionalbiasestowards
threaten-ingstimuli,bothinnormalfunctionandinanxiety.Whileresearch
hasexaminedtheroleoftop-downfactorsthatarenon-emotional
innature(fore.g.,searchingformatchingGaborpatches)andtheir
interactionwithbottom-upprocessingofemotionalstimuli(for
e.g.,task-irrelevantemotionalfacesinthebackground),veryfew
studieshaveexaminedtop-downfactorsthatarethemselves
emo-tionalinnature(e.g.,cuesindicatinganupcomingthreateningface)
andtheireffectonperception.Hence,wediscussconceptualand
methodologicalissuesintheresearchliteraturethatarisefroman
exclusivefocusonbottom-upfactorsinunderstandingprioritized
perceptionofthreateningstimuli.Wethendiscusstheimportance
ofendogenous,emotion-related‘top-down’factors,suchas
expec-tationsand prior knowledge regarding threat,in guiding basic
humanperception.Wealsodiscussemergingevidencethat
under-scorestheimportanceofendogenousprocessingintheperceptual
prioritizationofthreateningstimulibothinnormalfunctionandin
anxiety.Finally,wehighlighttheimportanceofshiftingthe
empha-sisfromstimulus-driventotop-downmechanismsaswellastheir
interactionwithbottom-upmechanismsinthestudyofthe
percep-tualprioritizationofthreateningstimulibothinnormalfunction
andinanxiety(Mohanty&Sussman,2013)
Thehumanvisualsystemisconstantlybombardedwith
infor-mation.Thelimitedcapacityofthis systemmakesitimpossible
toprocessallincominginformation(Tsotsos,1990).Asaresult,
stimulientering thevisualfield competeforneural
representa-tion(Desimone&Duncan,1995;Tsotsos,1997).Todealwiththis
overwhelmingexcessofinformation,thevisualsystembiasesthe
competitionbetweenstimulitowardspreferentialrepresentation
of themost relevant stimuli (Desimone &Duncan, 1995).This
biasingprocessisafunctionoftwomechanisms:abottom-up, sen-sorydrivenmechanismthatselectsstimulibasedontheirphysical salience,andatop-downmechanismwithvariableselection cri-teria,whichselectsstimulibasedonexpectations,knowledgeand goals.Unliketop-downmechanisms,bottom-upmechanismsare thoughttooperatebyautomaticallyshiftingresourcestosalient visualstimuli.For example,stimuli thatcreate alocal disconti-nuityinthevisualenvironment,suchasabruptoccurrenceofa newobject(Jonides&Yantis,1998),suddenmotionandlooming (Abrams&Christ,2003;Franconeri&Simons,2003),andluminance contrastchanges(Enns,Austen,DiLollo,Rauschenberger,&Yantis,
2001)aregivenmorepriority
Similarly, emotional stimuli are considered another class of stimulithatarehypothesizedtobeprocessedinabottom-up man-ner.Forexample,invisualsearcharrays,snakesandspidersare detectedfasterthanflowersandmushrooms(Ohmanetal.,2001); andangryfacesaredetectedfasterandmoreefficientlythan neu-tralandhappyfaces(Eastwood,Smilek,&Merikle,2001;Tipples, Atkinson,&Young,2002).Threateningfacesarealsoprocessed ear-lierandreceivemoreperceptualelaborationcompared toother facialexpressions(Schuppetal.,2004).Furthermore,saccadic reac-tiontimesarefastertowardsanemotionalcomparedtoneutral facesandbodypostures(Bannermanetal.,2009),aswellastowards emotionalcompared toneutral scenes(Nummenmaa,Hyona, & Calvo,2009).Similarly,negativewordsaredetectedmore accu-rately(Dijksterhuis&Aarts,2003;Nasrallah,Carmel,&Lavie,2009) andmorequickly(Dijksterhuis&Aarts,2003)thanpositivewords Attentionalprobesappearinginthesamelocationasthreatening facesaredetectedfasterthan probesappearingin theopposite location(Armony&Dolan,2002;Mogg&Bradley,1999;Pourtois, Grandjean,Sander,&Vuilleumier,2004)
Itishypothesizedthatemotionalstimuliareprioritizeddueto theirsalience,asproposedbyappraisal,constructivistand, dimen-sional theories of emotion (Barrett, 2006; Brosch et al., 2010; Ellsworth&Scherer,2003;Russell,2003),ortheirphysical char-acteristics,asdemonstratedbyperceptualprioritizationofshapes associatedwiththreats(Larson,Aronoff,Sarinopoulos,&Zhu,2009; Larson,Aronoff,&Stearns,2007).Forexample,inonestudy, par-ticipantswereaskedtodetectandratethevalenceofadiscrepant threatening,happyorneutralschematicfaceinarraysof other-wise identicalfaces(Lundqvist&Ohman,2005).Theschematic faceswere manipulated suchthat three, two or one feature(s)
oftheschematicfaceconveyedemotion.Resultsshowedbetter visualsearchperformanceformorenegatively ratedfaces,even
ifonlyonefeatureconveyedemotion,indicatingthatthe threat-eningmeaningofthefacedrivesimproveddetection(Lundqvist& Ohman,2005).Ontheotherhand,researchershavehypothesized thatthesearchadvantageofthreateningcomparedtoneutralfaces maybeduetofeaturessuchasupturnedlipcorners,openeyes,or frowningthatcanbediscriminatedfromneutralfeatures(Calvo
&Nummenmaa,2008;Larsonetal.,2007).Thiscouldbebecause
ofthesalienceofthethreat-relatedfeatures,resultingfromtheir associationwiththeholisticfacialexpressiontheycomefrom(e.g., Cave&Batty,2006),orbecauseofphysicaldifferencesbetween features ofthreateningvs neutral facesregardlessof emotional meaning.Finally,someresearchershavehypothesizedthatitisthe configurationofthreateningfacialfeatures,suchasshapeand posi-tioningofthemouthrelativetonoseandeyesthataidsvisualsearch (Calder,Young, Keane, &Dean, 2000; Carey &Diamond,1977), othershave concludedthat specificfeaturesare responsiblefor improveddetection(Calvo&Nummenmaa,2008),andsome stud-ieshavepresentedresultssupportingbothpositions(Lundqvist, Esteves,&Ohman,2004)
Trang 33 Neural mechanisms involved in bottom-up
threat-perception
Attheneurallevel,thebottom-upprocessingofemotional
stim-uliisbelievedtobemediatedviatheamygdalaanditsinteractions
withthevisualcortices(Cisler&Koster,2010;Dolan,2002;Ohman,
2002,2005).For example, resultsfromstudiesusing backward
maskingparadigmssuggestthatfearfulfacesactivatetheamygdala
intheabsenceofconsciousawareness(Morris,Ohman,&Dolan,
1998;Whalenetal.,1998).Usinganevent-relatedfMRIparadigm
in which subjects fixatedona centralcue and matched either
twofearfulorneutralfacesortwohousespresentedeccentrically,
Vuilleumierand colleaguesexaminedthehypothesisthat
emo-tionandvoluntaryattentionreflectdistinctinfluencesthatdonot
interact(Vuilleumier,Armony,Driver,&Dolan,2001;Vuilleumier,
Richardson,Armony,Driver,&Dolan,2004).Theyfoundthatwhile
activityin thefusiformgyrus(FG), which isknownto respond
stronglytofaces,wasmodulatedbyvoluntaryattention,
amyg-dalaresponsestofearfulfaceswerenot(Vuilleumieretal.,2001)
Bottom-upappraisalofemotionalstimuliisalsoassociatedwith
greater connectivitybetweenthe amygdalaand limbicregions,
suchastheanteriorcingulatecortex(Comteetal.,2014)
The amygdala is thought to quickly detect relevant
stim-uli,includingthreateningstimuli (Cunningham&Brosch,2012;
Sander,Grafman,&Zalla,2003),viaaneuralpathway,sometimes
referred to as the‘low road,’that passes through thesuperior
colliculi and thethalamus, that does not requirecorticalinput
(LeDoux, 2000), and carries low-spatial frequency information
Thistheoryhasbeensupportedbyevidencedemonstratingthat
lowspatialfrequencyimagesoffearfulfacesproducemore
amyg-dala activation than fearfulimagesdisplayed with highspatial
frequency (Vuilleumier,Armony, Driver,&Dolan,2003)and by
evidencethatemotionalfacescanbeprocessedintheabsenceof
awarenessin a subjectwithalesioned striatevisualcortex (de
Gelder,Vroomen,Pourtois,&Weiskrantz,1999).Recentevidence
using humanintracranial electrophysiologicaldata showedfast
amygdalaresponses,beginningasearlyas74-msaftertheonset
offearful,butnotneutral orhappy,facialexpressions(
Mendez-Bertoloetal.,2016).Thelatencyoffearresponsesinamygdalawas
muchshorterthantheirlatencyinthevisualcorticesandreliedon
lowspatialfrequencyinformation.However,thistheoryhasbeen
challengedbyacompetingmodel,positingthatduringthe
pro-cessingofemotionalvisualstimuli,theamygdala’sprimaryroleis
tocoordinatecorticalfunctionanddetectsalientstimuli(Pessoa&
Adolphs,2010).Thismodel(discussedingreaterdetailbelow)has
beensupportedbyevidencedemonstratingthatemotionalfaces
onlyproduce greateramygdalaactivitywhenfacesare actively
attendedto (Pessoa, Kastner,&Ungerleider,2002), and by
evi-dencethatrapidfeardetectioncanrelyonhighspatialfrequency
information,suggestinginvolvementofcorticalvisualareas(Stein,
Seymour,Hebart,&Sterzer,2014)
Aftertheamygdalaevaluatesincominginformationas
threat-ening, it can boost processing in other brain regions, such as
thesensorycortices,viare-entrantfeedback(Vuilleumier,2005)
Hence, exogenously-driven perceptual prioritization of
threat-relatedinformationishypothesizedtoinvolvevisualprocessing
modulated by re-entrant feedback signals from the amygdala
(Anderson&Phelps,2001;Davidson,2002;Ohmanetal.,2001;
Ohman,2005;Vuilleumier&Pourtois,2007).Sincetheamygdala
bothreceivesinputs fromallsensorymodalitiesandprojectsto
numerouscorticalandsubcorticalareas,itiswellpositionedto
influenceanumberofprocessesandbehaviors(Fox,Oler,Tromp,
Fudge,&Kalin,2015;Freese&Amaral,2009;Holland&Gallagher,
1999).Supportingthetheorythatthis rich connectivityisused
duringthreat perceptionis evidencethat lesionsin thehuman
amygdalaleadtolessactivationoftheFGwhenviewingfearful
faces compared to healthy controls and participants with hip-pocampallesions(Vuilleumieretal.,2004)andalsoleadtoless activationintheinferiortemporalcortex,aregioncrucialforvisual recognition,inmonkeys(Hadj-Bouzianeetal.,2012).Furthermore, greaterconnectivitybetweentheamygdalaandsensoryregions hasbeenfoundduringthreatperception(Lim,Padmala,&Pessoa,
2009;Morris,Fristonetal.,1998;Pessoa,Gutierrez,&Ungerleider,
2002).Theseempiricalresultssupportclaimsofquickand auto-maticprocessingofsalientstimuli,andprovideanamygdala-based mechanismbywhichthreatstimulicouldbeperceptually priori-tized
Inadditiontoevidenceofanamygdala-drivenbottom-up pro-cessingofsalientstimuli,studiessuggestthataventralnetwork, comprising the temporoparietal junction (TPJ) and the ventral frontalcortex(VFC),helpstoreorientattentiontosalient incom-ingsensoryinformation outsidethecurrent focusofprocessing (Corbetta&Shulman,2002).Thisnetwork isrecruitedby infre-quentorunexpectedeventsthataresalient;fore.g.,invalidlycued targetsinthePosnertaskoroddballs.Studiesshowthatduring top-downattentionalguidanceactivityinTPJissuppressed(Shulman, Astafiev,McAvoy,d’Avossa,&Corbetta,2007;Shulmanetal.,2003; Todd,Fougnie,&Marois,2005)andinthepresenceofsalient non-targetsstimulusactivityinTPJincreases(Geng&Mangun,2011) Hence,the TPJand VFCfunction likecircuitbreakers that shift thefocus to salient but task-irrelevantstimuli, even in case of emotionalstimuli(Dolcos&McCarthy,2006).Thesestudies sug-gestadditionalbottom-upstimulus-drivenmechanismsbywhich threatscouldbeperceptuallyprioritized,anddemonstratea possi-bilityofinteractionsbetweentop-downandbottom-upprocesses viaabrainnetworkthatissensitivetobothkindsofprocessing
While anxiety is typically conceptualized as an anticipatory responsetofuturethreateningevents,fearistypicallythoughtof
astheresponsetoanimmediatethreat(Davis,Walker,Miles,& Grillon,2010;Grupe&Nitschke,2013;LeDoux,2015) Neverthe-less,perceptualprocessinginanxietyistypicallyconceptualized
asdriven bybottom-up processes (Mathews &MacLeod,1994; Ohmanet al.,2001).Empiricalstudiesexaminingperceptionof threatening stimuliin anxiousindividuals, like thestudiesthat examinethesephenomenainhealthyindividuals,tendtoutilize tasks that exogenously drive perceptionand attentionthrough theuseofunanticipatedortask-irrelevantstimuli.Commontasks employedtostudy thisphenomenon present emotionalstimuli that ‘popout’amongstnon-emotional stimuli (Fox etal.,2000; Ohmanetal.,2001),areperipheraltofixation(Mogg&Bradley,
1999),appearrapidlyinstreamofimages(Arend&Botella,2002),
or are irrelevant to the task at hand (Williams, Mathews, & MacLeod,1996)
Experimentalresultssuggestthatcomparedtohealthycontrols, individuals withclinical anxiety(Klumpp&Amir, 2009; Mogg, Millar,&Bradley,2000;Ohmanetal.,2001),dispositional anxi-ety(Eysenck,Derakshan,Santos,&Calvo,2007;Mogg&Bradley,
1999;Richards,French,Johnson,Naparstek,&Williams,1992),and experimentallyinduced anxiety(Lim &Pessoa,2008;Robinson, Letkiewicz, Overstreet, Ernst, & Grillon, 2011) detect or orient towards threatening stimuli more quickly Other studies have foundnodifferenceintheinitialorientationtothreat,buthave demonstratedthatindividualdifferencesinanxietyincreasedwell timeandthetimerequiredtodisengagefromathreatening stim-ulus (Fox, Russo, Bowles, & Dutton, 2001; Yiend & Mathews,
2001).However,there is some empiricalevidence demonstrat-ingthatanxietycanbothfacilitateengagementwiththreatening stimuliandslowdisengagementwiththreateningstimuli(Koster,
Trang 4McMenamin,Greischar,&Davidson,2011),suggestingthat
anx-ietyinfluencesbothearlierandlatersensoryprocessesinvolved
in threat perception Finally, recent studies of soldiers
experi-encingacutestressors,suchascombat,showthat avoidanceof
threat,ratherthanabiastowardsthreatspredictssubsequentPTSD
symptoms(Wald,Shechneretal.,2011;Wald,etal.,2011).These
studiessuggestthatsituationallyinducedanxietymayinfluence
therelationshipbetweenorientationtothreatandfutureanxiety
symptoms
The well-documented, bidirectional relationship between
attentional biases tothreat and anxiety(Van Bockstaele et al.,
2014)hasledtothedevelopmentofcognitive-biasmodificationof
selectiveattention(CBM-A),aprocedurewithdemonstrated
thera-peuticpromise,andAttentionBiasModificationTreatment(ABMT),
atreatmentforanxiety.Bothofthesetechniquesarebasedon
cog-nitivebehaviouralmodelspositingthatcognitivebiasescanleadto
anxietydisorders,andthereforealteringattentionalbiasescould
subsequentlyreduceanxietysymptoms.ReviewsofbothCBM-A
andAttentionBiasModification(ABM)haveshownthese
proce-duresreduce anxietysymptomsand vulnerability toanxietyin
adults(MacLeod&Clarke,2015;MacLeod&Mathews,2012)andin
children(Eldaretal.,2012).Furthermore,meta-analysesof
stud-iesexaminingtheimpactofCBMandABMTonanxietysymptoms
hasdemonstratedthatthesetreatmentsareeffective(Hakamata
etal.,2010;Hallion&Ruscio,2011).Ameta-analysisoftheefficacy
ofABMTonclinicalanxietydemonstratedthatmorepatientswho
receivedthistreatmentnolongermetdiagnosticcriteriacompared
topatientsincontrolconditions(Linetzky,Pergamin-Hight,Pine,&
Bar-Haim,2015)
Different types of anxiety (e.g dispositionalvs situationally
induced)caninteract,impactingperceptualbiasesforthreatening
images.Forexample,anxietyinducedbyanupcomingexamination
increasedapre-existingtendencyforthosehigherindispositional
anxietytorespondmorerapidlytotargetsfollowinga
threaten-ingstimulus(MacLeod&Mathews,1988).Similarly,inindividuals
highintrait-anxiety,anegativemoodmanipulationledtogreater
interferencefromanxiety-relatedwordsonanemotionalStroop
task(Richardsetal.,1992).However,somestudieshavefounda
differentpatternof interaction.For example,whileparticipants
highintraitanxietyrespondedmoreslowlytothreateningwords
onanemotionalStrooptaskưindicatingthatattentionhadbeen
capturedbythesethreateningdistractorsưunderstress,trait
anx-ietynolongerinfluencedresponsetimes(Mogg,Mathews,Bird,&
Macgregor-Morris,1990).Asubsequentstudysuggeststhatwhile
transientstressorsmaywashoutdifferencesbetweenhighandlow
anxiousindividuals,chronicstressorsexaggeratethedifferencesin
attentionattributedtotraitanxiety(Mogg,Bradley,&Hallowell,
1994).Therefore,payingattentiontothetypeofstressorathand
couldresolvethedifferencesbetweenstudiesthatfindthatinduced
anxietyeitherincreasesordecreasesthreatbiases
Overall,clinical,dispositionalandsituationallyinducedanxiety
areassociatedwithfasterdetectionofthreateningstimuli.This
per-ceptualprioritizationofthreatinanxietyisattributedtoattentional
capture by the stimulus or automatic processing of
threaten-ingstimuli (Ohmanet al.,2001; Robinson,Charney, Overstreet,
Vytal,&Grillon,2012;Robinsonetal.,2011).Studiesthat
exam-inedbrainactivitywhileunanticipatedortask-irrelevantstimuli
exogenouslydriveperceptionandattentiondemonstrateincreased
amygdalaand visualcorticalactivityfor fearedstimuli in
anxi-ety(Lipka,Miltner,&Straube,2011;Straube,Mentzel,&Miltner,
2005) It is hypothesized that these perceptual enhancements
share similarities with exogenous stimulus-driven mechanisms
andaremediatedviaamydalarfeedbackintovisualsensoryregions
(Pourtois,Schettino,&Vuilleumier,2013)
Otherstudieshavedemonstratedthatveryearlysensory pro-cessingisboosted inclinically anxiousindividuals(Knottetal.,
1994),andinchildrenhigherindispositionalanxiety(Woodward
etal.,2001).Threateningstimulihavebeenshowntoactivatethe amygdalamoreforanxiousthannon-anxioussubjects,inclinical, dispositionalandexperimentallyinducedanxiety(Bishop,Duncan,
&Lawrence,2004;Calder,Ewbank,&Passamonti,2011;Etkin& Wager,2007;Etkinetal.,2004;Larson,Ruffalo,Nietert,&Davidson,
2005).However,theamygdaladoesnotworkinisolation.Arecent studydemonstratedthatunderthreatofshock,greaterfunctional connectivitybetweentheamygdalaandthedorsolateralprefrontal cortex(DLPFC)predictedfasterthreatdetection,andwaspositively associatedwithtraitanxiety(Robinsonetal.,2012).Otherstudies havefoundthatindividualswithanxietydisordershadless func-tionalconnectivitybetweentheamygdalaandtheDLPFCcompared
tohealthycontrolswhilerestingorviewingthreateningfaces(Birn
etal.,2014;Prater,Hosanagar,Klumpp,Angstadt,&Phan,2013) Furthermore,inonestudy,theconnectivitybetweenDLPFCand amygdalacorrelatednegatively withmeasuresofsocial anxiety (Prateretal.,2013).Together,thesestudiessuggestthatdifferent kindsofanxietyinfluencetherelationshipbetweentheamygdala andthefrontalcortexindistinctways
Whiletheliteraturedescribingtheimpactofanxietyon per-ceptionconsistentlydemonstratesabiasforthreateningstimuli, preciselywhenthisbiascomesintoplayremainsunclear.Sinceone
ofthecorefeaturesofanxietyisatendencytomakeinaccurate pre-dictionsregardingthelikelihoodandcostsoffuturenegativeevents (Grupe&Nitschke,2013),theeffectofanxietyonthreatperception maystartbeforestimuluspresentationandmayinvolvetop-down factorssuchasgoals,expectationsandpriorknowledge.Therefore,
togainacompleteunderstandingofhowanxietyimpactsthreat detection,itisnecessarytoexaminetheimpactoftop-down pro-cessingonthreatperceptioninanxiety
Overall, studies of psychological and neural mechanisms involvedin perceptionof emotionalstimulihavereinforcedthe viewthatemotionalsalience-related,bottom-upeffectsare invol-untaryandnotunderthecontrolofattention(Vuilleumier&Driver,
2007).However,thisresearchraisesmethodologicalissues First,themajorityofstudiesexaminingtheinfluenceof emo-tionalstimuli onattentionhave usedtasks inwhich emotional stimuliappearunexpectedly,suchasmodificationsofaperipheral
orexogenouscuingtask(Armony&Dolan,2002;Holmes,Green,& Vuilleumier,2005;Keil,Moratti,Sabatinelli,Bradley,&Lang,2005; Mogg&Bradley,1999; Mogg,McNamaraet al.,2000;Stormark
&Hugdahl,1996,1997).Thedotprobeparadigmisavery com-monlyusedtaskinwhichbothathreateningandneutralstimulus arepresentedsimultaneouslyandperipherally,andoneofthem
isfollowedbyanattentionalprobe(Holmesetal.,2005;Mogg& Bradley,1999;Mogg,McNamaraetal.,2000).Afacilitatedresponse
toprobesthatappearatthesamelocationofthreatinformation (validtrial),incomparisonwithresponsestoprobesatthe oppo-sitelocationofthreatinformation(invalidtrial),isinterpretedas vigilanceforthreat
Secondly,bottom-upprocessingofemotionalstimulihasbeen showntointeractwithtop-downfactorssuchasgoalsand task-relevance While bottom-up processing of emotional stimuli is adaptivewhentheyarerelevanttoourwell-being, itisequally adaptivetoignorethesestimuliandstaytask-focusedwhenthey posenodanger.Hence,adaptivebehaviorrequiresconstant inter-actionbetweentop-downgoalsandbottom-upprocessing.Studies usingparadigms in which emotionalstimuli aretask-irrelevant
Trang 5becausetheyareprocessedautomatically,leadingtoimpaired
task-relevantperformance.Forexample,task-irrelevantemotionalfaces
slowreactiontimes(Vuilleumieretal.,2001)anddecreaseaccuracy
(McHugo,Olatunji,&Zald,2013).Thepresentationofemotional
stimuliexogenouslyorasdistractorsinexperimentalparadigms
hascontributedtotheviewthatemotionalstimuliareprocessed
involuntarilyinabottom-upmannerandareimmunetotheeffect
attentionorcognitivecontrol
However,studiesalsoshowthatstrongasitmaybe,bottom-up
processingofanemotionalstimulusisalsosusceptibletotop-down
control For example, happyand threateningfacial expressions
have been shown to capture attentionwhen theyare the
tar-getofsearchbutnotwhen theyareinopposition totaskgoals
(Hahn&Gronlund,2007;Williams,Moss,Bradshaw,&Mattingley,
2005).Thisindicatesthatinadditiontostimuluscharacteristics,
top-downgoalsguidetheefficiencyofemotionalfacialexpression
search.Similarly,rewardandpunishmentcanmodulate
bottom-upcaptureofattention(Engelmann&Pessoa,2007)anddistractor
inhibition(DellaLibera&Chelazzi,2006).Formoredetailed
cov-erageontheinteractionbetweentop-downgoalsandbottom-up
processingofemotionalstimuliwewouldreferreaderstomore
comprehensivereviewsonthistopicbyAue,Chauvigne,Bristle,
Okon-Singer,&Guex,2016;Pessoa,2009;Pessoa&Ungerleider,
2005andPessoaetal.,2002;Pessoa,Gutierrezetal.,2002
Neuralevidencealsoindicatesthatbottom-upsubcortical
pro-cessingof emotionalstimuliissusceptible totop-downcontrol
Forexample,amygdalaanditsinfluenceonthevisualcortex,is
impactedbytop-downfactorsliketask-context andattentional
control(Pessoa&Adolphs,2010;Pessoa,2008).Amygdalaresponse
is modulatedvia top-downinputfromprefrontalbrain regions
duringemotionalconflict(Etkin,Egner,Peraza,Kandel,&Hirsch,
2006)and reappraisal(Ochsner,Bunge,Gross,&Gabrieli,2002;
Ochsneretal.,2004;Phan,Wager,Taylor,&Liberzon,2004);for
areviewsee(Ochsner&Gross,2005).While somestudieshave
arguedthatamygdalaresponsetothreateningstimuliis
indepen-dentofvoluntaryattention(e.g.Vuilleumieretal.,2001),these
studiestendtousetasksinwhichthreateningstimuliarepresented
inanunexpectedmanner,andhavenotexaminedthecontributions
top-downfactors,suchasthoseimplementedviaprojectionsfrom
theprefrontalcortextotheamygdala.Hence,PessoaandAdolphs
(2010)proposeanalternativemodel,whichunderlinesthe
numer-ousconnectionsbetweentheprefrontalcortex,thevisualcortex,
theamygdalaandothersubcorticalstructures,andpositsthatthe
amygdalaisprimarilyinvolvedinthecoordinationofcortical
pro-cessingratherthanjustthedetectionofthreat
Theinteractionbetweenbottom-upemotionalprocessingand
top-downfactorsalsoplaysanimportantroleinanxietyasoutlined
bytheattentionalcontroltheory(Eysencketal.,2007).Thistheory
positsthattraitanxietyincreasestheattentiongiventothreatening
stimuliandimpairsattentionalcontrol.Inotherwords,trait
anxi-etyimpairstop-downguidanceofattentionandboostsbottom-up
processesrelatedtothreatdetection.Morespecifically,according
toattentionalcontroltheory,traitanxietyimpairstheefficiency
withwhich non-threatening stimuli are processed, rather than
alwaysimpactingperformance.Thisisconsistentwithstudiesthat
foundthataccuracy(Calvo,Eysenck,Ramos,&Jimenez,1994;Ikeda,
Iwanaga, & Seiwa,1996; Markham& Darke, 1991) or reaction
timewasnotnegativelyimpactedbyanxiety(Bishopetal.,2004;
Comptonetal.,2003;Whalenetal.,1998).Attentionalcontrol
the-oryalsopositsthattheimpactoftraitanxietyonperformanceis
exacerbatedasdemandsontheexecutivecontrolincrease(Ashcraft
&Kirk,2001;Eysenck,1985)
Finally, in addition to evidence indicating that emotional
bottom-up factors constantly interact with top-down factors,
researchincreasinglyshowsthattop-downfactorsplayavitalrole
inperception(Barrett&Simmons,2015;Summerfield&deLange,
2014).Perceptualdecision-makingisheavilyinfluencedbyfactors thatoccurpriortophysicalencounterwiththestimulus,suchas, expectationsregardingwhatiscontextuallyrelevantorlikely.This
isexemplifiedbyfasterandmoreaccuraterecognitionofobjects thatoccurinfamiliarcontexts(Bar,2004;Brattico,Naatanen,& Tervaniemi,2002;Enns&Lleras,2008),hence,aloafofbreadis identified moreaccurately thana drum inthekitchen (Palmer,
1975).Morerecently,researchisshowingthatemotionaltop-down factorscanalsoinfluenceperception(e.g.,Sussmanetal.,2016; Sussman,Szekelyetal.,2016).Inthebrain,top-downfactorssuch
asexpectation,context,attention,andlearninghavebeenshown
toinfluenceamygdalaactivity.Theamygdalaisoneofthemost highlyconnectedregionsofthebrainandshowsconnectivity con-sistentwiththatofa‘hub’region(Barbas,1995;Stephanetal., 2000;Swanson,2003;Young,Scannell,Burns,&Blakemore,1994) indicatingthatitiswellsituatedtoinfluenceprocessinginother regions
In summary, while much has been learned regarding the bottom-up factors involved in the perceptual prioritization of emotionalstimuli,increasingevidenceisshowingthat1)studies examiningattentionalandperceptualbiasesforemotional stim-ulihavelargelyutilized paradigmsthatcapitalizeontheuseof bottom-upprocesses,2)bottom-upperceptionandrelated neu-ralmechanismsaresensitivetotop-downinfluence,3)top-down factorsplayacriticalroleinhumanvisualperception.Together, theselinesofevidenceunderscoretheimportanceofexaminingthe roleoftop-downprestimulusbiasesintheprirotizedperceptionof threateningstimuli
In contrastto bottom-upprocesses, top-down processesare endogenous and driven by contexts or goals According to the top-down perspective, visual perception involves a process of hypothesis testing in which predictive perceptual models are proposedbasedonpriorknowledgeandincomingsensory infor-mationis compared tothese predictedmodels(Gregory,1968; Summerfieldetal.,2006).Therefore,pastknowledgeand expe-rience createexpectationsof whatis relevantor likely,helping facilitatethespeedandaccuracyofsubsequentperceptual judg-ments This expectation takes the form of predictive neural representationsthatmaybebasedonperceptualtemplatesthat consistofimportantdiscriminatingfeatures(Neisser,2014)used
toaidstimulusrecognition
These predictive representations are implemented via two importanttop-downmechanisms:1)byanattention-related pri-oritizationofstimulusprocessing basedontherelevanceofthe stimulustogoalsand2)byanexpectation-relatedinterpretation
of stimulus based on thelikelihood of encountering an antici-patedstimulus(Summerfield&deLange,2014;Summerfieldetal.,
2006).Thefunctionoftop-downattentionistoallocatecognitive resourcesbasedontherelevanceorsalienceofastimulusgiventhe currentcontext.Commonmanipulationsofattentionbytop-down processesinclude spatialattention,feature-basedattention,and object-basedattention(Kanwisher&Wojciulik,2000).For exam-ple,priorknowledgeofthetargetstimuluslocationenhancesthe detectionofstimuliattheattendedlocation(Carrasco,Ling,&Read,
2004;Posner,Snyder,&Davidson,1980),evenwhenattentionis
‘covert’(i.e.intheabsenceofsaccadestoattendedlocations) Sim-ilarly,top-downspatialbiasingtowardsthelocationreducesthe distractingeffectsofsalientstimuliatotherlocations(Theeuwes, 1991;Yantis&Jonides,1984).Incontrasttoattention,theeffect
ofexpectationisoftenstudiedbymanipulatingthelikelihoodof theoccurrenceofastimulus.Studieshaverobustlydemonstrated thatresponsestovisualstimuliarefacilitatedbytheconditional
Trang 6probabilityofoccurrence ina given context.Objectsare
recog-nized morequickly ina context in which theyarelikely tobe
found(Gold&Shadlen,2007;Heekeren,Marrett,&Ungerleider,
2008).Researchalsodemonstratesthatobjectsinfamiliaror
pre-dictablecontextsarerecognizedfasterandmoreaccuratelythan
objectsseeninunpredictablecontexts(Bar,2004;Bratticoetal.,
2002;Enns&Lleras,2008);forexample,aloafofbreadis
iden-tifiedmoreaccuratelythanadruminthekitchen(Palmer,1975)
Additionally,humansintegrateandweighpriorknowledgeabout
likelihoodand uncertaintyincombination withcurrent sensory
informationinperceptualdecision-makingfollowingBayes’
the-orem(Bach&Dolan,2012).Incontrast,unexpectedvisualobjects
inacomplexsceneareoftendetectedmoreslowlyandwithmore
errors(Biederman,Mezzanotte,&Rabinowitz,1982)
While threateningstimuli cantakeus bysurprise, we often
detectthesestimuliwithincontextsorfollowingcuesthat
indi-cateanupcomingthreat.Implicitandexplicitenvironmentalcues
directustostimulithatarerelevantorlikelygiventhecontext,
subsequentlyimprovingperception.Forexample,acontextsuch
asadenseforestpathinColoradocancreateexpectationsof
see-ingabear,oranovertcue,suchasasignwarningthatafloorwas
recentlywashed,encouragesustolookforslipperyspots,resulting
infasterdetectionoftheexpectedstimulus.Emotionaland
moti-vationaltop-downfactors(e.g.searchingforthreatoranticipating
reward)havebeenshowntoinfluencetargetdetection.When
emo-tionalstimuli are task-relevant,in other words,when theyare
prioritizedbothbytop-downandbottom-upprocesses,detection
ofthesestimuliareimproved.Forexample,happyand
threaten-ingfacialexpressionsareprioritizedwhentheyarethetargetof
search,butnotwhentheyareinoppositiontotaskgoals,(Hahn
&Gronlund,2007;Williamsetal.,2005).Furthermore,cues
indi-catinganupcomingthreat-relatedperceptualdecisionimprovethe
sensitivityandspeedofsubsequentperceptualdecisions(Sussman
etal.,2016;Sussman,Szekelyetal.,2016),specificallyincaseof
subsequentfearfulfaces(Sussman,etal.,2016).Thesestudies
indi-catethat,inadditiontostimuluscharacteristics,emotion-related
top-downgoalsguidetheefficiencyoffacialexpressionsearch,and
canimprovetargetdetection
Top-downprocessescouldimprovethreatperceptionby
guid-ing attentionto a spatiallocation, or toa specific feature.For
example, ona visual search task, cues correctly predictingthe
spatiallocationandthreatvalueoffacesimprovedreactiontime;
performanceimprovedbothwhenspatialcueswereaccurateand
whencuesaccuratelypredictedanangryface,demonstratingthat
endogenousprocesses relatedtobothspatialand feature-based
attentioncanenhancethreatdetection(Mohanty,Egner,Monti,
&Mesulam, 2009).Additionally, ona cued word identification
task,emotionalwordsweremoreaccuratelyidentifiedthanneutral
words,whileemotionaldistractorshadnoimpactonperformance,
suggestingthatwhendirectedtolookingforaspecificemotional
stimulusviacues,perceptualprocessingofthatemotional
stim-ulusisenhanced(Zeelenberg,Wagenmakers,&Rotteveel,2006)
Thearousal-biasedcompetitiontheorysuggestsamechanismby
whichtop-downprocessesmayperceptuallyprioritizeemotional
stimuli.Itpositsthatemotionalcuesincreasearousal,biasing
selec-tiveattentiontowardperceptionofthestimulirelevanttothegoal
athand(Mather&Sutherland,2011)
Aftersensoryinformationhitstheretinaitisprocessedin
hier-archicallyorganizedregionswithincreasinglevelofabstractness
andcomplexitybeforea perceptisformed(Deco&Rolls,2004;
Tanaka,1996).Downstream(higherorder)brainregionsfeed infor-mationbacktoupstream(lowerorder)regions,influencinghow informationisprocessed.Thesefeedbackprojectionsoutnumber thefeedforwardprojectionsinmoststagesofthehierarchy,and thereforearelikelytohaveamajorinfluenceontheprocessingof incominginformation(Angeluccietal.,2002).Sinceattentionand expectationaretwotop-downinfluencesthatmayplayacrucial roleinperceptualbiasestowardsthreateningstimuli,thisreview willfocusonthesetwofactors
Top-down modulation of perception impacts most known stagesofvisualinformationprocessing,eveninbrainregionsthat processbasicvisualinformation,suchasV1(Li,Piech,&Gilbert,
2006;Motter,1993;Roelfsema,Lamme,&Spekreijse,1998).Infact, top-downmodulationhasbeenfoundtooccurevenbeforethe sen-soryinformation reachesthecortexin thesubcorticalregionof lateralgeniculatenucleus(McAlonan,Cavanaugh,&Wurtz,2008; O’Connor,Fukui,Pinsk,&Kastner,2002);forreviewsee(Gilbert
&Li,2013).Top-down modulationismore obviousin extrastri-ateareas(V2/V3andV4)(McAdams&Maunsell,1999;Nienborg& Cumming,2009),andinthemedial(Womelsdorf,Anton-Erxleben,
&Treue,2008)andventralvisualstreams(Chelazzi,Miller,Duncan,
&Desimone,1993).Theeffectofattentionandexpectationonvisual corticalactivityprior tostimulusonset hasbeendemonstrated
inmultiplehumanstudies(Esterman&Yantis,2010;Peelen, Fei-Fei,&Kastner,2009;Stokes,Thompson,Nobre,&Duncan,2009; Summerfieldetal.,2006).For example,usingacued face/house discriminationtask, onestudy demonstratedincrease of blood-oxygen-leveldependent(BOLD)signalinobject-category-specific visualcorticalareasduringexpectation(Esterman&Yantis,2010) Anticipationincreasesprestimulusneuronalactivityinsensory anddecision-relatedneurons(Kastner,Pinsk,DeWeerd,Desimone,
&Ungerleider,1999;Ress,Backus,&Heeger,2000;Summerfield
&de Lange, 2014) For example, studiesshow that neurons in the inferior temporal lobe that encode the expected stimulus showincreasedactivationfollowingapredictivecue(Erickson& Desimone,1999).Similarly,neuronsinmedialtemporallobe (sen-sitivetoobjectmotion)areactivatedpriortoapredictedmotion stimulus(Albright,2012;K.Sakai&Miyashita,1991).Prestimulus BOLDsignalinextrastriatevisualcortexisassociatedwith sub-sequentdecisionsregarding whethersubjectsreport seeingthe Rubin’svaseillusionasafaceoravase(Hesselmann,Kell,Eger,
&Kleinschmidt,2008),andface-relatedcueselicitincreasedBOLD signalinfusiformfacearea(FFA)priortofacestimulusonset(Bar
etal.,2001;Esterman&Yantis,2010;Puri,Wojciulik,&Ranganath,
2009).Inarandomdotclassificationtask,BOLDsignalinmotion sensitivevisualcortexpriortostimulusonsetpredictsthesubject’s response(Hesselmann,Kell,&Kleinschmidt,2008).Anotherstudy examiningtheprestimulusoscillatoryactivityovermotorcortex foundthatbothendogenousexpectation(withoutexplicitcue)and expectationinducedbyexplicitcuesbiasesthestartingpointof decision-relatedactivitybeforetheaccumulationofsensory evi-dence(deLange,Rahnev,Donner,&Lau,2013)
StudiesexaminingtheensembleactivitypatternsofBOLDsignal haveshownthattop-downattentiontoatargetactivates target-specific representations in shape-sensitive visual areas (Peelen
etal.,2009), andbrain regionsinvolved inolfactoryperception (Zelano,Mohanty,&Gottfried,2011),indicatingapreparatorybias favoringtheattendedstimulusovercompetingones
Increasedprestimulusactivitymayreflectincreasedattention priortostimulusonset,therebyimprovingsubsequentdetection (Hesselmann, Sadaghiani, Friston, &Kleinschmidt, 2010) Alter-natively,accordingtosequential samplingmodelsofperceptual decision-making,likethedriftdiffusionmodel(Ratcliff&Smith, 2004;Ratcliff,1978),increasesinprestimulusactivitymayreflecta biasorshiftinthestartingpointforevidenceaccumulationtowards
aspecificdecisionboundary,ormayreflectachangeintherateof
Trang 7Behav-iorally,studieshaveshownthatapredictedstimulusisassociated
withfasterreactiontime,higheraccuracy,andhigherperceptual
sensitivitycompared tounpredictedstimuli(Bar,2004;Geisler,
2008;Polat&Sagi,1994)
In additiontosensoryareas, top-downmodulationof visual
processing involves prefrontaland parietal areas For example,
top-down biasing of attention in space involves a network of
frontoparietal regions that include the intra-parietal sulcus in
the posterior parietal cortex (PPC) and the frontal eye fields
(FEF),theanteriorcingulatecortexandsupplementarymotorarea
(ACC/SMA), and thethalamus and superiorcolliculus (Corbetta
& Shulman, 2002; Gitelman et al., 1999; Kastner, De Weerd,
Desimone, &Ungerleider,1998; Kastneret al., 1999;Mesulam,
1981,1999; Reynolds,Chelazzi,&Desimone,1999).Thisspatial
attentionnetworkishypothesizedtoformanintegratedsearch
templatecombiningthespatialcoordinatesandtherelevanceof
the anticipated stimulus to bias visual neurons in preparation
for thesearch process (Egner,2008; Gottlieb, 2007; Thompson
&Bichot,2005).Brainregionsinvolvedwithassessingthe
moti-vational value of a stimulus include neurons in the inferior
parietallobuleandtheintra-parietalsulcus(Bushnell,Goldberg,
&Robinson,1981; Mountcastle,Lynch,Georgopoulos, Sakata, &
Acuna, 1975; Sugrue, Corrado, & Newsome, 2004) and limbic
regionssuchasamygdala(Pessoaetal.,2002;Pessoa,Gutierrez
etal.,2002;Vuilleumier&Driver,2007).However,whetherthese
regionscommunicateisunclear.Thecingulategyrusmaybea
con-duitforinformationonmotivationalsalienceusedbythespatial
attentionnetwork(Mesulam,VanHoesen,Pandya,&Geschwind,
1977), as the limbic parts of the cingulate gyrus send
projec-tionsto frontoparietal regions and posterior cingulateneurons
signalrewardoutcomesassociatedwitheyemovements(McCoy,
Crowley,Haghighian,Dean,&Platt,2003)andpreferencesguiding
visualorienting(McCoy&Platt,2005)
While most studies have focused onthe brain mechanisms
of bottom-up perception of emotional stimuli, newer evidence
is beginning to uncover the brain circuitry that is involved
in top-down guidanceby emotional information In one study,
endogenous guidance of attention wasmanipulated by
predic-tive cuesoffering both probabilistic information related tothe
locationof a subsequentlypresented stimulus,and information
regardingtheemotionalsalienceofthatstimulus(Mohantyetal.,
2009).Spatiallyvalidcuesenhancedtargetdetection.Inaddition,
cuesaccuratelypredictingangryfacetargetswereassociatedwith
fasterresponsesthanuninformativecues,indicating an
endoge-nousmediationofimprovedtargetdetection,drivenbyemotional
cues.Functionalimagingshowedthatpriortothestimulus
pre-sentation,spatiallyinformativecuesactivatedthefrontoparietal
spatialattentionnetworkincludingtheintra-parietalsulcusand
FEF,aswellasFG.Cuespredictingangryfacesalsoactivatedbrain
regions associated with emotional processing, including limbic
areas,suchastheamygdala.Additiveeffectsofspatialand
emo-tionalcueingwereidentifiedintheintra-parietalsulcus,FEFand
FGindicatingthatcuesactivateregionsinvolvedindirectingspatial
attentionpriortoarrivalofthethreatareactivatedinpreparation
Theseregionsalsohadincreasedconnectivitywiththeamygdala
followingangryfacecues.Thisstudydemonstratesthat
prestimu-lusthreat-relatedcueselicitamygdalainputtothespatialattention
networkandinferotemporalvisualareas,therebyfacilitatingthreat
detection
Separatefromtheeffectsofattention,expectationsregarding upcoming targetscanenhancetheirperception(Summerfield& Egner,2009).Accordingtothe‘predictivecoding’ theory,rather thanpassivelyabsorbingsensoryinput,thebrainactivelypredicts whatiscoming,generatingaprestimulustemplateagainstwhich observed sensory information is matched (Summerfield et al., 2006;Zelanoetal.,2011).InanfMRIstudyinwhichhumansubjects decidedwhethervisualobjectswerefacesornot,predictiveneural representationsrelatedtofaceswerereportedinmedialprefrontal cortex(mPFC;Summerfieldetal.,2006).Interestingly,perceptual decisionsaboutfaceswereassociatedwithanincreaseintop-down connectivityfromthemPFCtoface-sensitivevisualcortices, includ-ingFFA,consistentwiththeideathattheprefrontalcortexcodes forthepredictedrepresentationsandsendstop-downsignalsthat guidethesensoryregionsincollectingrelevantevidencetomake theperceptualdecision.Usingmultivariatepattern(MVP) analy-sesofprestimulusensemblepatterns,anotherstudyshowedthat target-specificensemblepatternsemergepriortoencounteringthe targetstimulusintheorbitofrontalcortex (OFC)andinsensory cortices.Furthermore,theseprestimuluspatternsreliablypredict subsequentbehaviouralperformance(Zelanoetal.,2011)
In a study thatexamined theimpactof threat compared to neutralprestimuluscuesonbrainactivityandsubsequent perfor-mance,threatcuesincreasedbothcue-andstimulus-relatedbrain activationandimprovedsubsequentstimulusdetection(Sussman
etal.,2016).Morespecifically,threatcuesresultedinalargerlate positive potential(LPP) and inincreasedsuperiortemporal sul-cus(STS)activity,bothofwhicharemeasuresofemotionalface processing.In addition,threatcuesspecificallyincreased amyg-dala activityfor subsequently presented threatening vs neutral faces.Furthermore, brain activity,as measuredby theLPP and STSactivity,predictedsubsequentimprovementinthespeedand precisionofperceptualdecisionsaboutthreateningfaces.These resultsdemonstratehowtop-down processingelicitedby pres-timulus threat-relatedcuescan enhancesubsequentperceptual decision-making.Ithasalsobeenhypothesizedthatthis enhance-ment maybedue toarousal-inducedrelease ofnorepinephrine intothelocuscoeruleusleadingtoincreasedlevelsofglutamate andnorepinephrineatthesiteofthegoal-relevantrepresentation, therebyenhancingtherepresentationofthegoal-relevantstimulus (Mather,Clewett,Sakaki,&Harley,2015)
Overall,whiletheneuralmechanismsinvolvedinprestimulus threat-relatedbiasesarerelativelyunexplored,emergingevidence indicatesthattop-downfactorsmayimpactthreatperceptionboth
bychangesinprestimulusactivityinsensoryregionsaswellas prestimulus biasing via templates instantiated in higher order regions(includingPPC,FEF,andotherprefrontalregions)and inter-actionsoftheseregionswithlimbicandsensoryregions
Top-downprocessesmayalsoplayacrucialroleinthe devel-opmentandmaintenanceofperceptualbiasesinanxietydisorders Anticipationofnegativefutureeventsisoneofthecardinalfeatures
ofanxiety.Forexample,peoplewithanxietytendtooverestimate boththelikelihoodofnegativeeventsoccurringandthecostof thesenegativeevents(Grupe&Nitschke,2013).Thus,apersonwith clinicalanxietyorspider-relatedfearstandinginaroomwith cob-websmighthavehigherexpectationofspidersbeingpresentand overestimatetheirdangerousnesscomparedtoanon-anxious per-soninthesameroom.Asaresultofthisoverestimation,anxious individualswillscantheenvironmentforspidersandwilldetect themfaster ifpresent.Researchershaveproposedthatfocusing
ontheanticipatoryphaseinanxietymaybeaneffectivestrategy
Trang 8anxietydevelopmentandmaintenance(Davisetal.,2010)
Accordingtothe‘uncertaintyandanticipationmodelof
anxi-ety,’anxietyinfluencesseveralcognitiveprocesses,twoofwhich
relatedirectlytothreatperception(Grupe&Nitschke,2013).First,
hypervigilance,orincreasedattentiontothreateninginformation
evenbeforeastimulusispresentedcanleadtobothfasterdetection
ofthreateningstimuliandamisinterpretationofneutralstimuli
Forexample,anxietycausedbythethreatofshockleadstofaster
detectionofnegativestimuli(Robinsonetal.,2011),interpretation
ofneutralfacesasbeingnegativeinsociallyanxiousindividuals
(Yoon&Zinbarg,2008)andinterpretationofambiguous
intero-ceptiveexperiences asbeingnegativein peoplehighinanxiety
sensitivity(Richards,Austin,&Alvarenga,2001).Second,inflated
estimatesofthreatprobabilityandthecostsofthreatscanleadto
improvedperformance(Paulus&Yu,2012),viaoverweightingof
lowprobabilityevents(Mukherjee,2010)
Recentevidenceprovidesdirectsupportfortheviewthat
anx-ietycanimproveperceptionbyinfluencing top-downprocesses
suchastop-down attention.Thisresearch shows improvement
inperceptualsensitivitydue topriorthreat-relatedinformation
isdependentonindividualdifferencesin traitanxietyand
cur-rentlevelsofinducedanxiety(Sussman,Szekelyetal.,2016).In
this study,two groups of participantsvarying in levels oftrait
anxiety(dispositionalanxiety)identifieddegradedemotionaland
neutralstimuliinacuedtwo-alternativeforced-choiceperceptual
task.Onegroupcompletedtheperceptualtasksinthepresence
ofthethreatofshock(highsituationallyinducedanxiety),while
theothergroupcompletedthesametaskintheabsenceofthreat
ofshock(lowsituationallyinducedanxiety).Individualdifferences
intraitanxietymoderatedgainsinperceptualsensitivity
follow-ingthethreatcue,suchthathighertraitanxietywasassociated
withlargergainsinperceptualsensitivityinthepresenceofshock
(Sussman,Szekelyetal.,2016)butworseperceptualsensitivityin
theabsenceofshock.Overall,resultsfromthisstudydemonstrated
thatdistincttypesofanxiety(dispositionalandinduced)interact
witheachotherininfluencinghowpriorthreat-related
informa-tionisusedinatop-downmannertoguideperception(Sussman,
Szekelyetal.,2016).Prestimulusthreat-relatedinformationcan
influenceperceptionbyeffectingattentionorexpectation,bothof
whicharehypothesizedtoinvolvedifferentpsychologicaland
neu-ralmechanisms(Summerfield&deLange,2014).Thecuesinthe
aforementionedSussman,Szekelyetal.(2016)indicatedwhatto
lookfor(threateningorneutralfaces)butthecuesdidnotprovide
informationregardingthelikelihoodoftargets
Aue and colleagues (2013, 2016) manipulated the
probabil-ityorlikelihoodofupcomingtargetstoexaminewhetherthreat
expectancy(inflatedestimatesofthreatprobability)impacts
detec-tionofaspiderorbirdsinindividualswithorwithoutspiderfear
(Aueetal.,2016;Aue,Guex,Chauvigne&Okon-Singer,2013).In
twostudies,theymanipulatedexpectancyviaaprestimuluscue
tellingparticipantstherewasa90%or50%likelihoodofseeinga
spiderorabird.Cuesindicatingthelikelihoodofspidersdidnot
haveasignificantimpactonthespeedofspiderdetectionfor
indi-vidualswithorwithoutspiderfear.However,prestimuluscues
regardingthelikelihoodofseeingabirdonthesubsequenttrial
leadtoobservabledifferencesinreactiontime,errorrates,pupil
diameterandheart rateforboth groupsof subjects(Aue etal.,
2016; Aue, Guex,Chauvigne& Okon-Singer,2013).These
stud-iesindicatethattop-downmanipulationofexpectanciesdoesnot
impactdetectionofthreateningstimulithewayitaffects
detec-tionofnon-threateningstimuli.Takentogether,theSussmanetal
(2016,2016)andAueetal.(2013,2016)studiesindicatethat
anxi-etyisassociatedwithdifferentialutilizationofattentionbutnot
probability-relatedinformation regardingupcoming threatening
stimuli
Making useof prior threat related information requires the maintenance of task-relevant representations online in work-ing memory to match against incoming stimuli (Sreenivasan, Sambhara, &Jha,2011).Because emotional representationsare maintainedwithgreatervividness(Bywaters,Andrade,&Turpin,
2004),theymaytaxworkingmemoryresourcesmorethan neu-tral internal representations Therefore, tasks that require the maintenanceofthreat-relatedinformation,orthatencouragethe unnecessary entry of threat-related information into working memorymayresult indeficitsforindividuals highin trait anx-iety(Stout,Shackman, &Larson,2013; Sussman,Szekely etal.,
2016).Traitanxietyisthoughttoparticularlyimpacttheefficiency
on tasks involving the inhibition function (supporting empiri-calresearchincludesCalvo&Eysenck,1996;Fox,2002;Yiend& Mathews,2001),theshiftingfunction(Eysencketal.,2007;Gopher, Armony,&Greenshpan,2000),and,toacertainextent,theupdating function(Duff&Logie,2001)
Neurally, anxiety is associated withreduced recruitment of regions involved in top-down control For example, predictive representationsofupcomingtargetstimuliaremaintainedin pre-frontalregions of thebrain, specifically,thedorsal and ventral medial prefrontalcortex(DMPFC &VMPFC;Summerfield etal.,
2006).Studiesshowthatanxietyisassociatedwithpoorer recruit-mentofDMPFC(Shinetal.,2005)anddorsolateralprefrontalcortex (DLPFC;Bishop,2009),possiblycontributingtoanimpaired abil-itytomaintainanddeploythreat-relatedperceptualtemplatesin theserviceofthreatperception.Inlinewiththis,lowtraitanxious individualshavebeenfoundtobenefitfromcuesprecedingavisual searchtask,whereasindividualshighintraitanxietyarenotable
tousethesecuesaseffectively(Berggren&Derakshan,2013).In
arecentstudy,decreasedperceptualsensitivityinhightrait anx-ietywasobservedforthreateningbutnotneutralcues(Sussman, Szekelyetal.,2016).Sincetheadverseimpactofanxietyon per-formancebecomesgreaterwithincreasingtaskdemandsonthe centralexecutive(Eysencketal.,2007),itispossiblethat main-tenanceofaperceptualsetforthreateningstimuliwhichmight
bemore complexmaybemore demandingthan maintaininga perceptualsetforneutralstimuli
Fewstudieshaveexaminedneuralmechanismsofthreatrelated guidanceofattentionorexpectationinanxiety.However, exami-nationofneuralactivityatrestorpriortostimulusonsetinanxiety providesclues intopotentialneuralmechanisms.Neuroimaging studies have demonstrated that the amygdala is more active forpeoplewithanxietydisorders comparedtohealthy controls (Furmarketal.,2002;Sakaietal.,2005;Sempleetal.,2000),and forpeoplewithashortvariantofthe5-HTtransportedgene com-paredtoindividualshomozygousforthelongvariant(Canlietal.,
2006),whenatrest.Anticipatoryamygdalaandanteriorcingulate cortex activityprior totreatmentpredictedtreatmentoutcome
8weekslater(Nitschkeetal.,2009).Inoneexperiment,subjects withsocialphobiawereaskedtoimaginegivingapublicspeech Individualswithsocialphobiahadhyperactivityinlimbicand par-alimbicregionscomparedtohealthycontrols(Lorberbaumetal.,
2004).Whileanticipatinggivingapublicspeech,sociallyanxious individualsalsoshowedincreasedlimbicactivationanddecreased striatalactivation(Boehmeetal.,2014),aswellasreduced func-tionalconnectivitybetweencorticalregionsinvolvedinemotion regulationandlimbicregions(Cremersetal.,2015).Furthermore, symptomseveritywasfoundtocorrelatewithchangesin activa-tionandconnectivity(Boehmeetal.,2014;Cremersetal.,2015) Overall,thesestudiesshowgreaterlimbicactivitypriorto stim-ulusonsetinanxietysuggestingthatanxietymayimpactthreat perceptionbychangesinprestimulusactivityinlimbicregions, possiblyleadingindividualswithanxietytointerpretcues regard-ingsalienceandthelikelihoodofupcoming threateningstimuli differentlythanindividualswithoutanxiety.Enhancedperceptual
Trang 9mayalsobeduetoenhancedsensory-perceptualfunctions,which
havebeenobservedinbothhightraitanxietyandinduced
anxi-ety(Robinson,Vytal,Cornwell,&Grillon,2013).Resultsfromone
studydemonstratethatthethreatofshockchangesneural
process-ingtoasensory-vigilancemodethatprioritizesthreateningstimuli
(Arnsten,2009;Shackmanetal.,2011).Finally,modelsof
decision-makingsuggestafewmechanismsthatcoulddrivetheperceptual
prioritizationofthreateningimagesinanxietybybiasingdecisions
towardsathreatenresponse(Sussman,Szekelyetal.,2016)
Overall,theroleoftop-downfactorsinthreatperceptionin
anxi-etyisnotwellunderstood.Whilegreateractivityinthreat-sensitive
limbicandsensorybrainregionsatrestandduringanticipatory
periodsinanxietysuggestsapossiblemechanismbywhichthreat
perceptioncouldbeprioritizedinanxiety,theimpactofanxiety
ontop-downattentionorexpectationofthreatisnotyetknown
Someempirical evidence supportsenhancements in perceptual
sensitivityduetopriorthreat-relatedinformation;however,these
perceptual benefits depend on the type of anxiety In
disposi-tionalanxiety,impairmentoftop-downmechanismsmaymake
utilizationandmaintenanceoftop-downthreat-related
informa-tionharder; whereas this information maybe more effectively
utilizedincaseofclinicalandsituationallyinducedanxiety
The perceptual prioritization of threatening stimuli, often
describedasabiasforthesestimuli,indispositional,clinicaland
inducedanxietyhasbeenobservedasfasterdetectionof
threat-relatedstimuli(Lim&Pessoa,2008;Mogg&Bradley,1999;Mogg
etal.,2000;Ohmanetal.,2001;Robinsonetal.,2011),orgreater
activationinfear-sensitivebrainregions(Bishopetal.,2004;Etkin
etal.,2004; Larsonetal., 2005).Thisperceptualadvantage has
generally beenstudied asa bottom-upphenomenon driven by
thephysicalcharacteristicsofthethreateningstimulus.Because
bottom-upprocesseswerethoughttodrivetheprioritized
percep-tionofthreat,experimentsdesignedtostudyabiasforthreatening
stimulihaveoftenreliedontasksthatonlytestedtheeffectsof
exogenous factors.However,top-downprocesses, suchas prior
knowledge,expectationsandgoals,influenceperception(Brosch
etal.,2010;Pessoa&Adolphs,2010).Furthermore,these
endoge-nous factors are of particular importance in anxiety, which is
characterizedbyexaggeratedandinaccurateestimatesofthe
prob-abilityandcostsoffuturenegativeevents(Grupe&Nitschke,2013)
Therefore,examiningtheimpactoftop-downfactorsonthreat
per-ceptioninanxietyisacrucialsteptowardssheddinglightonhow
basicprocessesofcognition,suchasperception,mayshapethe
developmentandmaintenanceofanxietyandrelateddisorders
Futurestudiesshouldfocusonexaminingthedifferentialimpact
ofthreat-relatedtop-downandbottom-upmechanisms(e.g.,cues
guidingone tolookforthreatening facesandthreatening faces
themselves)onperceptionandattention.Distinguishingtheimpact
ofprestimulusattentionfromtheimpactofprestimulus
expec-tationofseeingasalienttargetcouldprovidemorefine-grained
detailabouthowtop-downfactorsinfluenceperceptioninnormal
functionandinanxiety.Examinationofneuralandcomputational
modelswouldhelpelucidatethemechanismsimplementing
spe-cifictop-downandbottom-upfactorsinvolvedintheperceptual
prioritization of emotional stimuli For example, future studies
couldcomparepre-andpost-stimulusneuralrepresentationsof
emotionalvsneutralstimuliinvisualandprefrontalregionsofthe
brain,allowingustodeterminehoweachcontributestoperceptual
prioritizationofthreatinanxiety.Theuseofcomputationalmodels
wouldallowustoexaminethespecificmechanismsthatcontribute
totheperceptualprioritization
Furthermore,theimpactofothertypesoftop-downprocesses
onthreatperceptionshouldbeexamined.Forexample,sincewe typically caninferwhat kindsofthreats and rewardsaremore relevantorlikelydependingonthecontextwecurrentlyinhabit, exploringtheimpactofcontext onthreatperceptionwillallow formoreecologicallyvalidexaminationofhowemotionalstimuli areperceptuallyprioritized.Someworkhasbeenconductedinthis vein.Arecentstudydemonstratedthatnegativecontextsevoked
byrecallingareal-lifethreat(theBostonMarathonBombings)led
toanincreasedfalsealarmrateonashootingtask(Wormwood, Lynn,FeldmanBarrett,&Quigley,2016).Thisstudydemonstrates thatbystudyingtheimpactofcontext,wecanaddconsiderablyto ourunderstandingofhowthreatsareperceptuallyprioritized,and howneutralstimulimaybemisperceivedasthreateningin day-to-daylife.Theinteractionofsituationalcontexts(suchastheone describedabove),andinternalcontexts,suchasanxiety,orother moodsshouldalsobeexploredtogainamorecomplete under-standingofhowtop-downfactorsimpactperception.Whilesome researchhasbeendoneinthisarea,manyquestionsremain.One studydemonstratedthatafearfulmood,inducedviafilmclip,could speedreactiontimesoverandabovetheimpactoflow-levelvisual information(LoBue,2014).However,littleisknownabouthow pos-itivemoodsimpactthreatperception,orabouthowsituationaland internalcontextsinteractintheirimpactonthreat-perception Futureresearchshouldalsoaimtobetterisolatetheimpactof top-downfrombottom-upfactorsonthreatperception,asresults couldadvanceourunderstandingofhowthesefactorsinteractto perceptuallyprioritizeemotionalstimuli.Drawingthese distinc-tionsisespeciallycrucialwhenstudyingtheinfluenceofanxietyon perception,asanxietyisassociatedwithinaccurateestimatesofthe likelihoodandcostsoffuturenegativeevents(Grupe&Nitschke,
2013).Elucidatinghow individualdifferencesin anxietyimpact theinteractionbetweentop-down andbottom-up factors,both
intermsofbehaviouralperformanceandneuralprocessing,could providecluesabouthowbasicperceptualprocessesareassociated withclinicalsymptoms.This,inturn,mayprovidevaluablenew informationabouthowtocreatenewtreatmentsforclinical anxi-ety,andhowtoimproveexistingones.Forexample,arecentstudy foundthatdeliveringanABMTdesignedtoenhancevigilancefor threatpriortocombatexposureprotectedparticipants,reducing post-traumaticstressanddepression symptomsfollowing com-bat(Waldetal.,2016).Thisdemonstratesthatacknowledgingthe roleoftop-downprocessesinanxietycouldleadtonovelformsof therapy,somewhichcouldevenfunctionpreventatively
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