Cortical response of the ventral attention network to unattended angry facial expressions

13 Pages·2014·3.08 MB·English

by  Luis J. Fuentes

ORIGINALRESEARCHARTICLE
published:19December2014
doi:10.3389/fpsyg.2014.01498
Cortical response of the ventral attention network to
unattended angry facial expressions: an EEG source
analysis study
AlbertoInuggi1,FedericaSassi2, AlejandroCastillo2,GuillermoCampoy2,LetiziaLeocani3,
JoséM.GarcíaSantos4 andLuisJ.Fuentes2*
1BasqueCenteronCognition,BrainandLanguage,SanSebastián,Spain
2DepartamentodePsicologíaBásicayMetodología,UniversityofMurcia,Murcia,Spain
3InstituteofExperimentalNeurology,L’IstitutodiRicoveroeCuraaCarattereScientificoSanRaffaele,Milan,Italy
4ServiciodeRadiología,HospitalMoralesMeseguer,Murcia,Spain
Editedby: Introduction:Weusedanaffectiveprimetaskcomposedofemotional(happy,angry,and
AlanJ.Pegna,GenevaUniversity neutral)primefacesandtargetwordswitheitherpositiveornegativevalence. Byasking
Hospitals,Switzerland
subjectstoattendtoeitherthefaces’emotionalexpressionortotheglasses’shape, we
Reviewedby:
assessedwhetherangryfacialexpressionswereprocessedwhentheywereunattended
MarziaDelZotto,Universityof
andtask-irrelevant.
Geneva,Switzerland
AngelaGosling,Bournemouth Methods:Weconductedadistributedsourceanalysisonthecorrespondingevent-related
University,UK
potentialsfocusedontheearlyactivityoffaceprocessingandattentionnetworks’related
*Correspondence:
areas.Wealsoevaluatedthemagnitudeoftheaffectiveprimingeffect.
LuisJ.Fuentes,Departamentode
PsicologíaBásicayMetodología, Results:We observed a reduction of occipitotemporal areas’ (BA37) activation to unat-
UniversityofMurcia,Campus
tended compared to attended faces and a modulation of primary visual areas’ activity
Espinardo,30100Murcia,Spain
e-mail:[email protected] lateralization.Thelatterwasmorerightlateralizedforattendedthanforunattendedfaces,
and emotional faces were more right lateralized than neutral ones only in the former
condition.Affectiveprimingdisappearedwhenemotionalexpressionsofprimefaceswere
ignored.Moreover,anincreasedactivationintherighttemporo–parietaljunction(TPJ),but
notintheintraparietalsulcus,wasobservedonlyforunattendedangryfacialexpressions
at∼170msafterfacepresentation.
Conclusion:Wesuggestthatattentionalresourcesaffecttheearlyprocessinginvisualand
occipito-temporalareas,irrespectiveofthefaces’threateningcontent.Thedisappearance
oftheaffectiveprimingeffectsuggeststhatwhensubjectswereaskedtofocusonglasses’
shape,attentionalresourceswerenotavailabletoprocessthefacialemotionalexpression,
eventhoughemotion-relevantandemotion-irrelevantfeaturesofthefacewerepresented
inthesameposition.Ontheotherhand,unattendedangryfacesevokedapre-attentiveTPJ
activity,whichmostlikelyrepresentsabottom–uptriggerthatsignalstheirhighbehavioral
relevance,althoughitisunrelatedtotaskdemands.
Keywords: ventral attentional network, temporo–parietal junction, EEG source analysis, threatening facial
expressions,attentionmodulation
INTRODUCTION fearfulfacialexpression.Severalstudiesusingdifferentparadigms
Emotionaleventsplayacrucialroleinhowhumansinteractwith haveshownthateventhoughtheemotionalcontentofthestimu-
oneanotherandhowtheycanadapttochangingenvironments.To lusistask-irrelevant,itcapturesattentionandinterfereswiththe
fostersurvival,itisessentialthatthreateningstimulithatoriginate relevant task (Okon-Singer etal.,2007; Hart etal.,2010), delays
from other people or from the environment may be processed disengagement of attention (Georgiou etal., 2005), is detected
in a rapid and efficient manner. Many pieces of evidence show more easily than a neutral stimulus (Hansen and Hansen,1988;
thatthreateninginformationcanbeprocessedautomaticallyand Anderson, 2005; Calvo etal., 2006) and is better detected as a
independentlyofattentionorattentionalresources(Stenbergetal., T2 in the attention blink paradigm compared with a neutral
1995; Vuilleumier etal., 2001; for reviews, see Compton, 2003; T2 (Anderson, 2005). Further evidence for the automatic pro-
Vuilleumier, 2005). Moreover, this information processing can cessing of emotional expressions is derived from studies that
occurevenwithoutconsciousperception(forarecentreview,see explicitly manipulated the focus of attention by asking subjects
TamiettoanddeGelder,2010). to either attend to or ignore facial stimuli [e.g., Vuilleumier
Onecommonstimulususedtodemonstratehowthreatening etal., 2001; Anderson etal., 2003; Eimer etal., 2003; see Eimer
information can be prioritized and processed efficiently is the andHolmes,2007,forareviewof event-relatedpotential(ERP)
www.frontiersin.org December2014|Volume5|Article1498|1
Inuggietal. Processingunattendedangryfacialexpressions
studies]. For instance, Vuilleumier etal. (2001) presented two glassessothattheemotionalfacialexpressionwastask-irrelevant.
facesandtwohousesarrangedparafoveallyintheverticalorhor- Inaddition,whereasmanystudieshaveinvestigatedtheprocess-
izontal axis. Subjects had to compare the faces (faces-attended, ingof threateningstimuliusingfearfulfaces,wewereinterested
houses-unattended)ortocomparethehouses(faces-unattended, inextendingouraffectiveprimingstudiestoothernegativeemo-
houses-attended).Fearfulfaceswerecomparedwithneutralfaces. tionalexpression.Thus,angerfaceswereselectedforthepresent
The activation in the amygdala, the hallmark of emotional pro- study.Angerisfrequentlyexhibitedindailylifeasmuchasother
cessing,washigherwithfearfulthanwithneutralfaces.Notably, negativeexpressionssuchasfearandsadness,butfewstudieshave
activationintheamygdaladidnotdifferwhethertheparticipants usedthisemotionalexpressioninparadigmsthatusedattentional
paidattentiontothefacesortothehouses. manipulations.
Recentstudies,however,havechallengedtheideathatthepro- Onthebasisof ourpreviousresults,weexpectedanaffective
cessing of emotional information can occur without requiring primingeffectwiththeemotiontask,butnotwiththeshapetask.
a sufficient amount of attentional resources (Pessoa etal.,2002, However, as Okon-Singer etal. (2007) pointed out, it is neces-
2005;Holmesetal.,2003;OchsnerandGross,2005;Okon-Singer sarytodissociateattention-dependentprocessingfromautomatic
etal., 2007; Silvert etal., 2007; Sassi etal., 2014). For instance, processing (at least the“weak”notion of automaticity, Tzelgov,
Pessoa etal. (2002; see also Pessoa etal.,2005) found emotion- 1997;Pessoa,2005).Despitethelackofbehavioralprimingeffects,
related brain activity only when the subjects had to respond to whichmightdependontheavailabilityof attentionalresources,
thegenderofthefaces(easytask),butnotwhentheyhadtodis- is still possible that processing of the negative facial expression
criminate the orientation of two peripheral bars (difficult task). in the shape task occurs in a“strong”automatic way, indepen-
Holmesetal.(2003)comparedERPsbetweenfearfulandneutral dentlyofbothattentionalresourcesandtaskrelevance.Negative
facial expressions when the subjects had to compare two faces facialemotionalexpressionsmayberelatedtothreatandtherefore
(face attended) versus two houses (face unattended), with both theymaybebehavioralrelevantstimulithatrequireafastauto-
facesandhousesbeingsimultaneouslypresentedatdifferentspa- maticreactiontofostersurvival.Ifthatwerethecase,wewouldbe
tiallocations.Differencesbetweenthetwoemotionalexpressions abletodetectemotion-relatedbrainactivationevenwhensubjects’
wereobservedonlywhenfaceswereattended.Inarecentbehav- top–downattentionisallocatedtoanemotion-irrelevantfeature
ioral study, Sassi etal. (2014) used an affective priming task in of the face prime that requires fine-grained discrimination (the
whichaprimefaceshowingeitheranemotional(positiveornega- shape task). The rational for that hypothesis is the existence of
tive)oraneutralexpressionwasfollowedbyanemotionallyladen aneuralcircuitrycomprisingbothsubcorticalandcorticalareas,
target word (positive or negative). In the critical trials the tar- thatisinvolvedintherapidandautomaticdetectionofthreaten-
getwordcouldbeprecededbyafaceprimethatbelongedtothe ing salient stimuli, and that may play a crucial role for survival
sameaffectivecategoryofthetarget(congruentcondition)orto (Vuilleumier,2005).
a different affective category (incongruent condition). Affective Inthestudy,wecarriedoutdistributedsourceanalyses(Fuchs
priming was measured through congruency effects, that is, the etal., 1999) over the ERP generated by the face. Unlike dipole
differenceinperformancebetweenthecongruentconditionand analysis (Scherg and Von Cramon, 1985), which uses very few
the incongruent condition. Sassi etal. (2014) observed affective sourcesandneedsstrongapriorihypothesesabouttheircharac-
priming when the subjects’attention was allocated to the emo- teristics,thesourceanalysistechniquerepresentsthecorticalbrain
tional information (emotion task), and also, albeit of a smaller activitythroughtheintensityofalargenumberofcorticalgener-
size, when the emotion expression was made task-irrelevant by ators,providingamorerealisticsimulationofbrainfunctioning.
asking subjects to determine whether the face wore glasses (the Amongtheseveralapproachesavailabletosolvetheinverseprob-
glasses task). However, when the subjects were asked to deter- lem of reconstructing the cortical sources that generated the
mine whether the glasses were rounded or squared (the shape recorded scalp potentials, we opted for a well-established post-
task),theaffectiveprimingeffectvanished.Thisfindingwasprob- processing method (Inuggi etal., 2010, 2011a,b; Gonzalez-Rosa
ablyaconsequenceofthefactthattheshapetask(difficulttask) etal.,2013).ItemploysasLORETA-weightedaccurateminimum
requiredmoreattentionalmonitoringthantheglassestask(easy normmethod(SWARM)algorithm(Wagneretal.,2007),which
task),andthereforetherewerenotsufficientattentionalresources allowsforthelowreconstructionerrorofsLoreta(Pascual-Marqui,
as to process the emotional expression of the face prime (see 2002)andalsooutputsacurrentdensityvectorfieldthatcanlater
also Okon-Singer etal., 2007, for similar evidence using a cog- bepost-processed.
nitive load paradigm). A common feature of the studies that Wefocusedthenonthecorticalareasthatareinvolvedinthe
report attentional modulation of emotional processing is that processingof thefine-grainedfacialfeatures. Briefly,theprocess
the non-emotional task usually involves a high attentional load; of recognizing the static (identity, gender, familiarity) and the
therefore, sufficient attentional resources were not available to dynamic(emotionalexpressionsandgazedirection)characteris-
processtheemotionalcontentofthestimuli(Lavie,1995;Pessoa ticsof theobservedfacearethoughttorelymainlyonacortical
etal.,2002,2005;Okon-Singeretal.,2007;PalermoandRhodes, stream(Haxbyetal.,2000; PalermoandRhodes,2007)embrac-
2007). ing both the classical ventral stream (Ishai etal., 1999) and the
Thepresentstudyisafollow-upoftheSassietal.’s(2014)study, superiortemporalsulcus(STS).Theventralstreamoriginatesin
althoughonlytwotaskswereused:theemotionaltask,inwhich theoccipitalareasandpropagatesthroughtheoccipitalfacearea
subjects attended to the emotional expression of the face, and (OFA) and the fusiform face area (FFA). The FFA is specialized
the shape task, in which subjects attended to the shape of the in decoding fine-grained static facial characteristics (Kanwisher
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Inuggietal. Processingunattendedangryfacialexpressions
etal., 1997; Halgren etal., 2000; Holmes etal., 2003; Bayle and MATERIALSANDMETHODS
Taylor,2010),whiletheSTS,especiallyitsposteriorpart(pSTS),is SUBJECTS
involvedintheprocessingofdynamicfacialfeatures,suchaseye Twenty-eight healthy, young (mean age 22.1 ± 2.3 years, range
gaze,andindecodingtheemotionalinformationfromfacialfea- 19–30)subjectswithnohistoryofneurologicorneuropsychiatric
tures(Puceetal.,1998;Allisonetal.,2000;HoffmanandHaxby, disorderswererecruitedtoparticipateinthisstudy.Fourteensub-
2000; Saidetal.,2010). Previousstudieshaveobservedthatthat jects(11femalesand3males)participatedineachtaskcondition
FFA activates more with facial than with non-facial objects (see (emotion and shape). All subjects were right-handed according
Haxbyetal.,2000,forreview),andthereforeweexpectedreduced to their self-report and gave their written informed consent for
activation of that area in the shape task (focused on a non- participationinthestudy.
face feature) compared to the emotion task (focused on a facial
feature). TASK
To model the activation of these areas, we performed both Subjects were tested individually in a sound-attenuated room.
sourcesandsensorsanalysisincorrespondencetothemainERP A computer program generated by E-Prime 2 (Schneider etal.,
components.Besidesmodelingthetwomostlyinvestigatedearly 2002)controlledtheexperiment.Thestimuliwerepresentedona
components, the posterior P1 and the lateral occipito-temporal 17(cid:3)(cid:3) TFT monitor (screen resolution: 1024 by 768 pixels; back-
N170,wealsomodeledtheanteriorN1(Luoetal.,2010)andalater ground color: silver – RGB: 200, 200, 200) and participants
positive component, peaking around 230–250 ms, whose name responded via the keyboard. We used three grayscale pictures
andtemporallocationvarygreatlyacrossstudies(e.g.,VPPinLuo (4.5cmwideby7.7cmheight)ofhumanfacesasprimestimuli,
etal.,2010;P270inLiuetal.,2012).BothP1andN1components oneforeachfacialexpression(happy,angry,andneutral).These
havebeenassociatedwithafirststageofautomaticprocessingthat stimuli were taken from the NimStim Set of Facial Expressions
differentiatesnegativefacialexpressionsfrompositiveorneutral (Tottenhametal.,2009;thereferencecodesoftheselectedfacesare
facial expressions (Pourtois etal., 2004; Luo etal., 2010), which 20_M_HA_O,20_M_NE_C,and20_M_AN_O).Byusingphoto-
reflects an early negativity bias (Smith etal., 2003). The N170 editing software, we created two versions of each picture, one
componenthasbeeninvolvedinthedistinctionbetweenfacesand wearingroundedglasses,andtheotherwearingsquaredglasses.
non-faces stimuli (Bentin etal., 1996; Rossion etal., 2003; Itier As target stimuli, we used 36 Spanish words divided into two
andTaylor,2004;Luoetal.,2010).Astheaforementionedcompo- sets, one comprising 18 positive words, the other containing 18
nentshavebeenshowntobeaffectedbyaffectiveprocessinginan negative words. Mean valence ratings for the words of the two
earlyphaseofperceptionandattentionprocessing(Carretiéetal., sets ranged from 1.7 to 2.8 (M = 2.3) for positive words and
2004;EimerandHolmes,2007;Luoetal.,2010),theyconstitute from –0.9 to –1.8 (M = –2.3) for negative words, according to
themaingoalof ouranalysisof thefirst300mspostfaceprime a preliminary study (N = 124; scale ranging from –3 to +3;
onset. seeSassietal.,2014). Positiveandnegativewordswerematched
Sourceanalyseswerealsoemployedtoassesswhetherangryand forwordfrequency,familiarity,andwordlengthusingtheLEX-
non-angry (happy and neutral) expressions were processed dif- ESP database (Sebastián-Gallés etal.,2000). Each trial consisted
ferentlywhenattentionwasdirectedtoemotion-irrelevantfacial of the following sequence (the trial scheme is summarized in
features. Specifically,becausenegativeemotionalexpressionsare Figure1). First,a1000-msfixationpoint(aplussign)appeared
behavioral relevant stimuli, we expect activation in the ventral in the center of the screen followed by one of the three prime
attentionnetwork(VAN),whichissupposedtodetectbehavioral faces, which was presented for 200 ms. Then, after an interval
relevantbuttask-irrelevantstimuliandtoexertabottom–upmod- of 100ms(stimulusonsetasynchrony,SOA=300ms),atarget
ulation over the dorsal attention network (DAN; Corbetta and word was shown (in capital letters and black font) and subjects
Shulman,2002;Corbettaetal.,2008).However,becauseemotion-
relevantandemotion-irrelevantfeatureswerefoveallypresented,
wedidnotexpectanyreorientingprocessbytheDAN,whichis
responsiblefortop–downcontrolasitcontains,specificallyinthe
FrontalEyeFieldregion,thepropercircuitrytomovestheeyesto
theselectedtarget.Thus,wemaybeabletotestthehypothesisthat
theVANmightactivateindependentlyfromtheDANbyassess-
ing brain activity in both the temporo–parietal junction (TPJ;
VAN) and the intra-parietal sulcus (DAN). These networks are
consideredsupramodal(Macalusoetal.,2002;Greenetal.,2011)
andnotdirectlyrelatedtofaceprocessing.Becausetheirinvolve-
mentinbottom–upandtop–downcontrolisderivedmainlyfrom
functional magnetic resonance imaging (fMRI) studies, whose
temporal resolution is not enough as to be coupled with elec-
troencephalography (EEG) activation findings, their activation
time course will be investigated here in the temporal proximity
oftheclassicalERPpeaks,wherethefacefeaturedecodingprocess
FIGURE1|Sequenceofeventsandtimedurationintheexperiment.
isexpectedtooccur.
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Inuggietal. Processingunattendedangryfacialexpressions
indicated whether the word was positive or negative by press- Table1|Event-relatedpotentialcomponentsinvestigated,electrodes
ing the “n” or “m” key on the computer keyboard as quickly containedintheeightclustersused,andthewindowofinterestused
todefinethecomponent’speak.
and accurately as possible (this first response is referred to as
R1). Both prime faces and target words were presented cen-
Components Clustername Electrodesin Windowof
tered. The specific response-key mapping was counterbalanced
cluster interest
across participants. Immediately following R1, a double-choice
question appeared on the screen, and subjects were prompted
N1 L/RFrontal F3/4,FC3/FC4 80–130
to press, with no time limit, the key (“z” or “x”) that corre-
P1 L/ROccipital PO7/8,PO3/4,
sponded to the correct answer (hereafter, R2). In the emotion
condition,subjectswereaskedwhethertheprimefacewasneutral O1/2,Oz,POz
oremotional(theemotiontask),whereasintheglasses’shapecon- N170 L/ROccipito-temporal PO7/8,PO3/4, 130–190
ditiontheywereaskedwhetherthefaceworeroundedorsquared P7/8
glasses(theshapetask).Thewholeexperimentincluded72con-
N170 L/RTemporo–parietal P5/6,CP5/6
gruent trials, 72 incongruent trials, and 144 neutral trials. In
P240 Allthepreviouslydefinedclusters 220–260
congruent trials, the prime face and the target word belonged
to the same affective valence, either positive, as it happened in
happy-positive trials (N = 36) or negative, as it happened in the temporo–parietal region. These eight cluster measures were
anger-negative trials (N = 36). In incongruent trials, a prime subjectedtostatisticalanalyses.Infurtheranalysis,thetwooccipi-
face with different valence preceded the target word, as it hap- talclustersweremergedintoasinglecluster,anditsactivationwas
penedinhappy-negativetrials(N =36)andanger-positivetrials expressedintermsofthelateralizationofitsmedial–lateralcenter
(N=36).Inneutraltrials,aneutralprimefaceprecededthetarget ofgravity,calculatedwiththefollowingformula:
word, as it happened in neutral-positive (N = 72) and neutral-
negative(N =72)trials.Targetwordsweredrawnfromeachset COGx= (a∗PO8+b∗PO4+c∗O2−a∗PO7−b∗PO3
at random, with the constraint that each word appeared in two
−c∗O1)/2∗(a+b+c)
congruenttrials,intwoincongruenttrialsandinfourneutraltri-
als.Ashortpracticeblockof18trialsprecededtheexperimental
where a,b,c represent the medial–lateral coordinates of those
trials.
electrodesina10–20extendedsystem.
EEGRECORDINGSANDPREPROCESSING
SOURCEANALYSIS
Electroencephalography was recorded using 59 scalp channels
A preliminary ICA (Hyvarinen, 1999) was performed on ERP
mountedontoanelasticcap(ActiveCap,BrainProductsGmbH),
data,whichallowedforthedecompositionofthesignaltonoise-
according to the 10–20 international system, with the refer-
normalizedindependentcomponents(ICs). OnlythoseICsthat
ence located close to the vertex. The EEG signal was amplified
showedanSNRbelow1acrossallintervalsofinterest(from–250
(BrainAmp,BrainProductsGmbH),digitized(1000Hzsampling
to 300 ms with respect to the facial onset) were removed from
frequency),andfiltered(0.1to40Hz).Theelectrodeimpedance
the ERP data (Inuggi etal., 2011a,b). The source activity was
was kept below 5 K(cid:2). Four additional electrodes were placed
reconstructed using the cortical current density (CCD) model
to monitor the left/right and horizontal/vertical ocular activity.
withaconductorvolumedefinedbya3-compartmentboundary
Theeyemovements’artifactswerecorrectedwithanindependent
elementmethod(BEM),withconductivityvaluesof0.33-0.0042-
component analysis (ICA) Ocular Artifact Reduction algorithm
0.33S/m(Fuchsetal.,2002),derivedfromtheFSLMNItemplate
(VisionAnalyzer,BrainProductsGmbH).TheERPswereobtained (www.fmrib.ox.ac.uk/fsl),dimensionsof91×109×91andavoxel
byaveragingtheEEGepochsfrom–250to+300mswithrespectto size of 2×2×2 mm. The sources number (6899) and positions
faceonset,usingthefirst200msforbaselinecorrection.Datawere
wereobtainedbysamplingthecortex(5mmwide),withtheirori-
finallyre-referencedusingacommonaveragereferenceapproach.
entationsfixedperpendiculartothecorticalpatchtheyoriginated
from,andtheirintensitieswerecalculatedusingtheSWARMalgo-
ERPCOMPONENTSDEFINITION
rithm(Wagneretal.,2007).TheCCDwasreconstructedwiththe
According to previous studies, we focused on the P1 and N170
CurryV6software(NeuroscanInc.,Herndon,VA,USA).
components and also on N1, which peaks in frontal regions at
∼100 ms. Additionally, our data revealed a late positive deflec- ROIdefinition
tion, peakingat∼240ms, thatwasalsoinvestigated. Fourpairs Cortical activity was calculated in seven pairs of right and left
of sensorsclusters,whoseamplitudewascalculatedasthemean regionsofinterest(ROI)involvinglateralfusiformgyrus(BA37),
amplitudeoftheirconstituentsensors,weredefinedtomodelthe posteriorsuperiortemporalsulcus(pSTS),TPJplusinferiorpari-
ERPcomponents.Ineachsubjectandforeachexperimentalcon- etallobule(TPJ+IPL),intraparietalsulcus(IPS),middlefrontal
dition,theamplitudesofcomponents’peakswerecalculatedasthe gyrus(MFC),inferiorfrontalgyrus(IFG),andprimaryvisualarea
maximumpositive/negativedeflectionswithinthetimewindows (V1).Inanadditionalanalysis,thetwoV1ROIsweremergedinto
specified in Table1. To better compare ERP results with source a single ROI,and its activation was expressed in terms of later-
analysisresults,afurthercluster,conventionallynotinvestigated alization of its medial–lateral center of gravity, calculated as is
inpreviousstudies,wasdefinedfortheN170periodthatcovered explainedlateron.
FrontiersinPsychology|EmotionScience December2014|Volume5|Article1498|4
Inuggietal. Processingunattendedangryfacialexpressions
Regionsof interestweremanuallydrawnontheMRIimages STATISTICALANALYSIS
using the Curry software internal anatomical atlas and previous The effects of the between-subjects factor task type (emotion
research as references. TPJ+IPL ROI was created starting with task, shape task) and the within-subjects factor face expression
the strict TPJ definition of Mort etal. (2003) but also included (angry, happy, or neutral) and hemisphere (left and right) over
the inferior parietal lobe, like most studies that investigate the TA within each area and period were analyzed with a mixed
VAN and that located their activations around these areas. Its analysisofvariance(ANOVA).TheKolmogorov–Smirnovtestwas
resultingcenterofgravitywillclarifymorespecificallytheanatom- usedtoexaminethenormaldistributionof thedata,and,when
ical localization of this activation. To take into account possible appropriate,theGreenhouse–Geissercorrectionwasapplied.The
between-subjects electrodes’slight montage misallocation, ROIs significancelevelofthemaineffects(tasktype,emotionalexpres-
were enlarged (5 mm wide) and then smoothed (2 mm wide). sion, and hemisphere) and their interactions were corrected for
ROIsareillustratedinFigure2. multiplecomparisons(14ROI×3periods)usingafalsediscovery
rate(FDR)approach,butusingamoreconservativeversion(Ben-
ROIactivity jaminiandYekutieli,2001)comparedtostandardFDR.According
Threeperiodswereinvestigated:L100,whereN1andP1areactive, toitsformula(α/(cid:3)i=1..k(1/i),wherei=42isthenumberofmul-
L170,whichcorrespondstotheN170peak,andL240,whichcor- tiple comparisons and α = 0.05 is the predetermined p-value),
respondstoourlatepeak.Withintheseperiods,themeancortical wereportonlythesignificantp-valuesbelow0.0112.Becausethe
activationofeachROIwasseparatelycalculatedusingthefollow- numberofmultiplecomparisonswaslowerintheERPanalysis(8
ingprocedure: (i)withineachlatency, theintensityof allof the cluster×3periods),thecorrectedthresholdwas0.0132.Thesize
activesourcescontainedintheROIweresummed;(ii)thelatency effectswerereportedthroughtheη2 value.Posthoccomparisons
p
withthehighestvaluewasdefinedasthepeaklatency(PL);and(iii) ofwithin-subjects(facialexpression)andbetween-subjects(task
a40ms-lengthtemporalwindow,centeredonthatpeak,wasused type)factorswereperformedwithpairedandunpairedt-tests.The
tocalculatetheareatotalactivity(TA)withineachperiodofeach multiplepairwisecomparisonsoffacialexpressionswereadjusted
area,aswaspreviouslydescribed(Inuggietal.,2011a;Gonzalez- withtheBonferronicorrection.
Rosa etal., 2013). This procedure was performed separately for To provide the ERP equivalent of our source analysis results,
eachROI,thusallowingustotakeintoaccounttheonsetdiffer- a mixed ANOVA, analyzing the effects of task type and face
encesofnearlysimultaneouscomponents(e.g.,P1andN1)andto expression, was also performed over the ERP electrode clusters
createperiodsofthesametemporallengthtoensurepropercom- that overlay the ROI of the sources significantly affected by our
parisons. Thelengthof thetimewindowwasselectedaccording experimentalfactors.
toapreviousstudy(Gonzalez-Rosaetal.,2013).
Theactivationsofcenterofgravity,decomposedinthemedial– RESULTS
lateral (CX), anterior-posterior (CY), and ventral-dorsal (CZ) BEHAVIORALDATA
positions,werecalculatedusingthefollowingformula(e.g.,CX): Trialswithincorrectresponsestothetargetword(R1;1.8and1.5%
fortheemotiontaskandtheshapetask,respectively),andtrials
CX = ((cid:3) s ∗X )/(cid:3) s , withincorrectresponsestotheto-be-attendedfacialfeature(R2;
ij ij ij ij ij
3.1and5.0%fortheemotiontaskandtheshapetask,respectively)
wereexcludedfromanalysis.Inaddition,weexcludedtrialswith
wheres istheintensityofthei-thsourceattimepointjandX is
ij ij
RTs below 200 ms (anticipations) or more than three standard
themedial–lateralpositionofthei-thsourceattimepointj.
deviation(omissions)fromthesubject’smeanforeachcondition
(1,90%). The mean RT for R1 in the emotion task was 790 ms
(SD = 144) for congruent trials (happy face/positive word and
angryface/negativewordtrials)and825ms(SD=164)forincon-
gruent trials (angry face/positive word and happy face/negative
wordtrials).Intheshapetask,themeanRTwas767ms(SD=173)
for congruent trials and 768 ms (SD = 155) for incongruent
trials. These means were submitted to mixedANOVA withcon-
gruency(congruent,incongruent)andtasktype(emotion,shape)
asfactors.Therewasamaineffectofcongruency,F(1,26)=9.75;
MSE =464;p=0.004;η2 =0.27,revealingthatresponseswere
p
faster for congruent than for incongruent trials (this difference
represents the affective priming effect, M = 18 ms). However,
thiseffectwasqualifiedbyacongruency bytasktype interaction,
F(1,26)=9.10,MSE=464,p=0.006,η2=0.26.PosthocFisher’s
p
leastsignificantdifference(LSD)tests(MSE=25411,df=26,479)
FIGURE2|Corticalareasinvestigated.IPS,intraparietalsulcus;pSTC,
posteriorsuperiortemporalsulcus;TPJ,temporo–parietaljunction;BA37, revealedsignificantcongruencyeffectfortheemotiontask(prim-
lateraltemporo–occipitalcortex;MFC,middlefrontalcortex;IFG,inferior ingeffect=35ms, p <0.001)butnoeffectatallfortheshape
frontalgyrus.Withindottedlines,isrepresentedthatpartofTPJwhich task(primingeffect=0.6ms,p=0.941).Results,thus,replicate
overlapswithIPSandpSTS.
thoseobtainedinourpreviousbehavioralstudy(Sassietal.,2014).
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Inuggietal. Processingunattendedangryfacialexpressions
Tosupportthegoodnessofourprotocol,weverifiedthatneither Effectoftasktype
themaineffectsof wordvalence,F(1,26)=1.56,p=0.222,and DuringL170,aneffectoftasktypewasobservedinlateralBA37
tasktype,F <1,northeirinteraction,F(1,26)=1.30,p=0.26, activity, [F(1,26)=7.93; p =0.011, η2 =0.26], whichwasless
p
werestatisticallysignificantwiththeneutralexpression.Analysis intense(Figure4)intheshapetask(M=2.28,SD=0.6μA/mm2)
oferrorrate(CR1)revealednostatisticallysignificanteffects. thanintheemotiontask(M=5.4,SD=0.5μA/mm2).
SOURCEANALYSISDATA Interactionbetweentasktypeandfacialexpressions
The group averages of the evoked potentials elicited by the two Asignificanttypetaskxfacialexpression×hemisphereinteraction
tasks, which merged the three emotional faces, are displayed in was observed in IPL+TPJ during L170, [F(1.518,39.45) = 6.41,
Figure 3. Table 2 summarizes the activation’s center of gravity p = 0.010, η2 = 0.23]. Post hoc analyses revealed that the type
p
coordinatesandPLvaluesoftheROIs,whereasignificanteffect task × facial expression was significant only for the right side,
ofeithertasktypeorfaceemotioncouldbeobserved. [F(1.81,37.06)=5.35,p=0.010,η2=0.218].Additionally,while
p
facialexpressionsdidnotdifferfromeachotherintheemotion
task,aneffectoffacialexpressionwasobservedintheshapetask
Table2|Talairachcoordinatesofactivations;center-of-gravityinright whenfacialexpressionshadtobeignored,[F(1.58,20.56)=12.06,
IPL+TPJROIatL170. p=0.001,η2=0.48],withhigheractivationtoangryfacialexpres-
p
sions (M = 8.1, SD = 1.1 μA/mm2) compared to both happy
Area Task Neutral Happy Angry
(M =5.8,SD=0.9μA/mm2,p=0.002)andneutral(M =6.1,
X Y Z X Y Z X Y Z SD=0.8μA/mm2,p=0.002)ones(Figure4,right; Figure5).
Thecenterof gravitypositionof corticalactivationinIPL+TPJ
RTPJ170 Emotion 49 –51 24 48 –49 23 49 –49 22 ROI,reported in Table 2, was located in close proximity to the
Shape 49 –51 29 48 –53 28 49 –50 23 TPJdefinedbyMortetal.(2003),asshowninFigure5.Wethus
will refer to it as TPJ activation. No modulation over the IPS,
FIGURE3|GroupaveragesofERPinemotion(solidline)andshape(dottedline)tasksinthefirst300msafterfacialstimuluspresentation.Forallthe
electrodes,theverticalscaleboundaryissetat+10μV.
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Inuggietal. Processingunattendedangryfacialexpressions
FIGURE4|EffectofemotionalexpressionandtasktypeatL170.(Left)TasktypeeffectsonrightlateralBA37.Nosignificantdifferenceswereobservedfor
facialemotion.(Right)RightTPJsensitivitiestoangryfacialexpressioninshapetaskonly.Onthey-axis,themeanactivityofeachROIintheL170time
windowisexpressedinμA/mm2.
FIGURE5|Theshapetask:increasedactivationinresponsetotheangryfacialexpression(right)comparedtohappy(center)andneutral(left)
expressionsintheTPJwithintheIPL+TPJROI(voxelsenclosedwithintheyellowborders)atL170.
pSTS,or middle and inferior frontal areas were observed at any clusterswasmodulatedbytasktype[F(1,26)=5.45,p=0.011,
latency. η2 =0.25],whichwasmoreright-lateralizedintheemotiontask
p
(M = 11.3, SD = 4.5 mm), than in the shape task (M = –0.9,
Lateralizationofvisualareaactivity SD = 3.8 mm). At ∼170 ms, the occipito-temporal cluster that
DuringtheP100component,themedial–lateralcenterofgravity overlays the lateral BA37 was not affected by the task type. In
(CX)of thevisualareaswasmorelateralizedtotherighthemi- therightoccipito-temporalcluster,whichshouldprovidetheERP
sphereintheemotion(M=–5,SD=0.9mm)taskcomparedto equivalentoftherightTPJactivation,asignificantinteractionwas
theshape(M=8.7,SD=2.1mm)task[F(1,26)=8.21,p=0.010, found between task type and facial expression in the occipito-
η2 =0.281;Figure6].Asignificanttasktype×facialexpression temporal cluster [F(1.52,21.13) = 5.20, p = 0.012, η2 = 0.24].
p p
interaction was observed in visual areas, [F(1.53,38.21) = 6.55, Nevertheless,wefoundatrend(p=0.065)versusamorenegative
p=0.010,η2 =0.18].Theeffectoffacialemotionontheactiva- peak to angry faces compared to neutral ones in the shape task
p
tionlateralizationwasobservedonlyintheemotiontask,withthe (Figure7). Nodifferencesemergedwithintheparieto-temporal
angry(M =12,SD=2.5mm,p=0.011)andhappy(M =10, cluster.
SD=2.2mm,p=0.010)facesmorelateralizedtotherighthemi-
spherewithrespecttotheneutralfaces(M =4.7,SD=2mm). DISCUSSION
NosignificantdifferencesemergedintheL240interval. In this study, the effect of a fine-grained, emotion-irrelevant,
discriminatory task on the early emotional faces processing was
ERPDATA investigatedbyreconstructingthecorticalgeneratorsofthescalp-
DuringtheP100component,themedial–lateralcenterofgravity recordedpotentials. Ourmainobjectivewastoevaluateif angry
of the cluster obtained by merging the right and left occipital expressions were processed differently from non-angry (neutral
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Inuggietal. Processingunattendedangryfacialexpressions
FIGURE6|VisualarealateralizationaroundL100.(Left)Theeffectoffacial emotionalfacialexpression(center)comparedtotheneutralfacialexpression
expressionandtasktypeonthemedial–lateralpositionoftheactivation’s (right)intheemotiontask.Onthey-axis,themeanactivityoftheROIinthe
center-of-gravity(COG).Thecorticalcurrentdensity(CCD)resultsofthe L100timewindowisexpressedinμA/mm2.
FIGURE7|ERPresults:(upperrow)effectoftasktypeoveroccipito-parietalcluster;(lowerrow)effectoffacialexpressionoveroccipito-parietal
clusterinemotion(left)andshape(right)tasks.
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Inuggietal. Processingunattendedangryfacialexpressions
andpositive)expressionswhenattentionwasdivertedtoanother results strongly suggest that our shape task succeeded in guid-
task.Weoptedtoengagesubjectsinafinediscriminationof the ing subjects’ attention away from any face feature, preventing
shape of the glasses worn by the face stimuli, a task that was any conscious monitoring of the emotional content of the face.
supposedtodeplete,accordingtoourpreviousbehavioralstudy, In the long debate over the pre-attentive automaticity of emo-
theattentionalresources(seeSassietal.,2014). Severalprevious tionalprocessing,ourresultssuggestthatanappropriatelevelof
studies assessed the interaction of attention and emotion when attention is needed to process emotional expressions. Although
emotion-relevant and emotion-irrelevant stimuli did not share presentedinthesamevisualfocus,thereducedBA37activityand
thesamegeometricalspace(Vuilleumieretal.,2001;Holmesetal., the loss of emotional selectivity of primary visual areas in the
2003).Becausetheredirectionofthesubject’sattentiontoanother shapetasksuggestthatsubjectspresumablyfocusedtheirattention
positionmayrepresentapotentialconfoundingissue,weoptedto justontheglasses’shapeandignoredtheunderlyingemotional
placeboththeemotion-relevantandemotion-irrelevantfeatures expression.
inthesamefovealposition,removinganyobstaclestotheauto- Thelateralizationoftheactivationsfoundinthepresentstudy
maticprocessingof emotionalfaceswhenaskedtoignorethem. deservesfurthercomments.Thelateralizationofemotionalpro-
In addition to investigating the peculiar processing of ignored cessing is still an open issue because the two main theories,
angryfaces,wewerealsointerestedingivinganeurophysiological supportingeithertheright-hemispherehypothesis(RHH;Borod
explanation for the loss of the affective priming effect observed etal.,1998;Bourne,2010)orthevalence-specifichypothesis(VSH;
in our behavioral results (Sassi etal.,2014, current study) when Mandaletal.,1991;Adolphsetal.,2001),havebeenquestionedby
subjectswereinvolvedinanemotion-irrelevanttask.Weconcen- more recent fMRI meta-analysis investigations (Fusar-Poli etal.,
tratedouranalysisonthecorticalareasinvolvedintheprocessing 2009;Sabatinellietal.,2011).Thebulkofevidenceshowsbilateral
ofthefine-grainedfacialfeatures,whicharesupposedtobehighly activationforemotionalfaceprocessinginmostemotion-related
modulated in a top–down manner by the observers’ attention, areas,althoughlateralizationmightbemodulatedbygender(see
makingitsprocessingnotpre-attentivebutstrictlyrelatedtothe forexampleWageretal.,2003).Inthepresentstudymost(22out
availability of attentional resources. Moreover, considering the of 28) of the subjects were women, and our data are consistent
highpriorityofaversivefacialexpressionsincapturingattentional with a previous EEG report specifically investigating the gender
resources, we also focused on the parietal areas that belong to effect over emotional face processing. Proverbio etal. (2006) in
both the ventral (TPJ) and the dorsal (IPS) attention networks factfoundmaximalP1amplitudeovertherightoccipitalcortex
and the partially overlapped frontal areas of the two networks, inbothgenders,consistentlywithourresultsshowingthatinthe
the inferior (IFG) and middle (MFG) frontal gyri (Fox etal., emotion task occipital activity around 100 ms was right lateral-
2006). ized.Thelackofarightlateralizationobservedinourdataduring
theN170mayappearinconsistentwiththewidelyacceptedright
THEEFFECTOFATTENTIONONTHEVENTRALSTREAM predominance of FFA in face processing (Kanwisher and Yovel,
Inthepresentstudy,weconfirmthattheventralstreamishighly 2006). However, this again agrees with Proverbio etal.’s (2006)
modulatedbytheobserver’sattention.Theactivityoftheoccipital findingsofarightlateralizationofN170onlyinmen.Incontrast,
areasat∼100mswasmorerightlateralizedintheemotiontask women exhibited a bilateral pattern. These results can help fos-
thanintheshapetaskand,morenotably,whensubjectsattended terbetterunderstandingoftheinconsistenciesintheliteratureon
to the facial expression, activation produced by emotional face therighthemisphereadvantageintheoccipito-temporalcortices
expressionswasmorerightlateralizedthanactivationproducedby whenprocessingfacesandconfirmtherelevanceofincorporating
neutralfaces.Suchselectivitydisappearedwhensubjectsattended genderinformation.
totheglasses’shape.
ConsideringthattheassessmentofFFAactivitythroughscalp ANGRYFACIALEXPRESSIONPROCESSING
recordings is widely questioned, as the area lies within the infe- Although both static and emotional features appeared under-
rior part of the temporal cortex, we created the lateral BA37 processedbycanonicalfaceprocessingcorticalareas,unattended
ROI because previous neuroimaging studies showed a correla- angryexpressionswereabletoactivatetheTPJ,acorticalexpanse
tionbetweentheN170EEGcomponent,calculatedbyelectrodes implicated in a wide spectrum of high-order cognitive func-
overlaying it and fMRI-derived FFA activity (Horovitz etal., tionsrangingfromsocialcognition(SaxeandKanwisher,2003)
2004; Sadeh etal., 2010), which suggests that surface electrodes to attention selection (Corbetta and Shulman,2002). The latter
may capture at least part of FFA activity. Additionally, electro- branchofinvestigationshowedthattheTPJispartoftheVAN,a
corticography studies have revealed that lateral BA37 is also fronto-parietalnetworkthat,duringfocusedactivities,isformally
involved in face processing (Rossion etal., 2003; Tsuchiya etal., involvedinre-orienting(shifting)attentiontostimulirelevantto
2008). At ∼170 ms, lateral BA37 activation was reduced in the the immediate goal. Nevertheless, because the attentional focus
shape task compared with the emotional task, which suggests covered a similar area in both tasks, no reorienting process was
that when subjects were asked to ignore the facial expression expected,asourIPSactivityalsoindicates.Thelatterisinfactpart
and just concentrate on the glasses’shape, the detailed face fea- of the DAN, which contains the proper circuitry to implement
tures might not have been very distinctive. This result agrees the focus reorienting, and was not modulated by our experi-
withpreviousfindingsthatreportlargeractivityinFFAforfaces mental conditions. The absence of any modulation over frontal
comparedtonon-faceobjects(Haxbyetal.,2000; Rossionetal., areas might be interpreted accordingly; the integration between
2003). Taken together, our behavioral and neurophysiological ventral and DANs, needed for attention re-orienting, occurs in
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Inuggietal. Processingunattendedangryfacialexpressions
suchaforementionedfrontalareaswherethetwonetworkshighly thatsubjectsfocusonwordonsetandthecorrespondingresponse
overlap(Foxetal.,2006). relatedtoitsemotionalvalence.
Thus, the present findings support the proposal that VAN
activation, at least in its parietal areas, might not exclusively be DIFFERENCESBETWEENSOURCESANDSENSORSANALYSIS
involved in attentional reorienting. It is consistent with more Inthepresentpaper,weaimedtoprovideanERP-equivalentof
recentreportsthatsuggestthatTPJactivitymightbetriggeredby theactivationsproducedbysourceanalysis.Wethusfocusedthis
bothexternalsensorystimuliandinternalmemory-basedinfor- analysisonlyonthetimewindowsandclustersthatsurroundthe
mation,thusprovidingbottom–upsignalstoothersystemsabout corticalareasaffectedbyourexperimentalconditions.ERPanaly-
relevant stimuli for further inspection (Cabeza etal., 2012). In sisfoundthatattendedemotions,comparedtoignoredemotions,
agreement with the present results, VAN activity has also been havetheiroccipitalP1peakmorerightlateralizedbutwasunable
observed when behaviorally relevant, rather than salient, stim- toassesstheselectivitytowardattendedemotionalfaces,whichdis-
uliarepresentedwhiletheindividualisengagedinanothertask appearedintheshapetask.Inasimilarmanner,ERPanalysiscould
(Corbettaetal.,2008). Accordingly, the activation of TPJ just detecttheinteractionbetweentaskandemotionsat∼170msin
when the unattended face was shown with an angry expression therightoccipito-temporalcluster,butitdidnotfindasignificant
suggeststhatnegativeemotionscanpre-attentivelyevokebottom– differencebetweenangryandnon-angryignoredfaces.Ofcourse,
upcorticalsignals,accordingtotheirbehavioralrelevance,even thecurrentERPapproachisonlyoneofmanypossibleapproaches.
when attention is focused on emotion-irrelevant features in a WearenotconcludingthatanotherERPanalysiswouldhavebeen
taskthatweassumedexhaustedtheattentionalresourcestopro- unabletolocatethesameeffectsfoundwithsourceanalysis.How-
cess the emotional content of faces. Because the ventral stream ever,evenif suchaneffecthadbeenencounteredinaclusteror
andSTSwerenotmodulatedbythedegreeof unattendedemo- in a channel (e.g., CP4 or CP6), it would have been impossible
tionalcontentandtheVANisconsideredasupramodalnetwork toclearlyattributeittooneoftheareasbeneathandclosetothe
(Macalusoetal.,2002; Greenetal.,2011)notabletodecodethe sensors cluster. Ideally, both pSTS and BA37 would have been
threatening pattern from facial expression, we suggest that TPJ validcandidates,andwecouldhavearguedthatbecausetheyare
activation might be triggered from other brain regions. Several partofthecorticalstreamsupposedlydeputedtoextractfacefea-
neuroimaging studies suggested that, in parallel with the corti- tures,theywouldhavepresumablyshownsuchfunctioningalsoin
cal stream (Palermo and Rhodes, 2007), a subcortical pathway, theattendedcondition,butthatdoubtwouldhavepersisted,and
that reaches the amygdala through fast and coarse subcortical theinvolvementof TPJcouldhavebeenjustoneof thepossible
inputsthatoriginateinthesuperiorcolliculusandfinallyproject hypotheses. Instead,sourceanalysis,whencalculatingthecenter
onto fronto-parietal areas, is thought to implement a brain cir- ofgravityofthelargeROIcoveringthetemporalandparietallobe,
cuitryspecializedinemotionalattention(Vuilleumier,2005).This indicatedtheTPJinvolvement.
circuitry,likelypartlymodulatedbytheattentionalfocus(Pour-
toisetal.,2013)isinvolvedintherapidandautomaticdetection METHODOLOGICALCONSIDERATIONSANDLIMITSOFTHEPRESENT
of negative facial expressions (for review; see Vuilleumier and INVESTIGATION
Pourtois, 2007), and it seems to play a crucial role in direct- The main limits of EEG source analysis are its high sensitivity
ing attention and information processing to threatening stimuli to artifacts, the low signal-to-noise ratio and the limited spatial
(Ohman and Mineka, 2001). Because reconstructing amygdala resolution.Toproperlyaddresstheselimits,weemployedacon-
activitywithEEGpresentsseveralaccuracylimitations,asitwillbe solidated methodological approach (Inuggi etal.,2010,2011a,b;
discussedlater,furtherstudiesthatintegrateEEGwithneuroimag- Gonzalez-Rosa etal., 2013), which has consistently proved to
ingtechniquesaresurelyneeded,butourdataareconsistentwith obtain results in line with the neuroimaging literature. We used
such a model. A previous MEG study showed in fact that the a seed-based analysis instead of a voxel-wise one because this
amygdalaactivatesasearlyas100msafterstimuluspresentation approachisoftenusedinbothEEGandneuroimaginganalyses,
(Streitetal.,2003), alatencyearlyenoughtotriggerTPJactiva- whenstronghypothesisoftheinvolvedbrainareasispossible.In
tionat∼150–170ms. ThepresentTPJactivationof ∼170msis fact, although the experimental task, seen as a whole, is brand
consistent with a recent ERP study that investigates the threat new, the areas involved in the investigated interval have been
detection advantage (Feldmann-Wüstefeld etal., 2011), which accurately described in the past as producing a consistent pic-
revealed that angry and happy expression processing started to turethatguidedandsupportedourROIselection.Weadopteda
differ at ∼160 ms. This suggests that angry faces may trigger a conservativeapproach,selectingROIsinareasontheoutersur-
fearmodulethatenablestheirrapidprocessingandrecruitaddi- faceof thebrainwherethespatialresolutionof theEEGsource
tionalattentionalresources,possiblybymeansof TPJ,asishere analysisismaximalandavoidingtheinvestigationof deepbrain
hypothesized. areas such as the proper FFA, orbitofrontal, para-hippocampal
In conclusion, within the VAN, TPJ activation at this early corticesandamygdala.Theseareaswerereportedinseveralneu-
latency primarily signals the behavioral relevance of a task- roimagingstudiesbuttheirreconstructionthroughEEGpresents
irrelevantaversivestimulus,irrespectiveofwhetherthatstimulus severalmethodologicalissues.EEGsourceanalysisaccuracyisin
requires a physical shift of attention (involving the dorsal net- facthighlycorruptedbythehugeanisotropyandinhomogeneity
work). The fact that such a trigger was not followed by an of the brain that blur the emerging signal when it is not mod-
actual over-processing of face features is likely due to the task eled by a proper volume conductor model. Deep sources are of
demandsthat,immediatelyafterfaceoffset(∼200ms),required coursemoreburiedwithinthebrainastheideallinesseparating
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