Luca
Tommasi
aDepartmentofNeuroscienceandImaging,‘G.d’Annunzio’UniversityofChieti-Pescara,Chieti,Italy
bDepartmentofPsychologicalScience,HumanitiesandTerritory,‘G.d’Annunzio’UniversityofChieti-Pescara,Chieti,Italy
cDepartmentofClinicalandExperimentalMedicine,NeuroscienceandCellBiologySection,PolytechnicUniversityofMarche,Ancona,Italy dRegionalEpilepsyCentre,NeurologicalClinic,“OspedaliRiuniti”,Ancona,Italy
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•Chimericanddichoticstimuliwerepresentedtotwosplit-brainpatients(D.D.V.andA.P.).
•Stimuliconveyedhappy/sadexpressionsandparticipantsjudgedtheiremotioncontent.
•Thetotalsplit-brainpatientD.D.V.neglectsvisualstimuliinthelefthemifield.
•A.P.showsaright-hemisphericdominanceinunimodalanalysis.
•ThevalencehypothesisisconfirmedinbimodalconditionsbyA.P.andthecontrolgroup.
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Articlehistory: Received2June2014
Receivedinrevisedform16June2014 Accepted18June2014
Availableonline24June2014 Keywords: Audio-visualintegration Split-brain Chimericface Dichoticstimulation Hemisphericasymmetry
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Hemisphericasymmetrieshavebeenwidelyexploredinboththevisualandtheauditorydomain,butlittle isknownabouthemisphericasymmetriesinaudio–visualintegration.Wecomparedtheperformanceof apartiallycallosotomizedpatient,atotalsplit-brainpatientandacontrolgroupduringtheevaluation oftheemotionalvalenceofchimericfacesanddichoticsyllables(anemotionalsyllableinoneearand whitenoiseintheotherear)presentedunimodally(onlyfacesoronlysyllables)orbimodally(facesand syllablespresentedsimultaneously).Stimulicouldconveyhappyandsadexpressionsandparticipants wereaskedtoevaluatetheemotionalcontentofeachpresentation,usinga5-pointLikertscale(from verysadtoveryhappy).Inunimodalpresentations,thepartiallycallosotomizedpatient’sjudgments dependedontheemotionalvalenceofthestimuliprocessedbytherighthemisphere,whereasthoseof thetotalsplit-brainpatientshowedtheoppositelateralization;intheseconditions,thecontrolgroup didnotshowasymmetries.Moreover,inbimodalpresentations,resultsprovidedsupportforthevalence hypothesis(i.e.,leftasymmetryforpositiveemotionsandviceversa)inboththecontrolgroupandthe partiallycallosotomizedpatient,whereasthetotalsplit-brainpatientshowedatendencytoevaluatethe emotionalcontentoftherighthemifaceevenwhenaskedtofocusontheacousticmodality.Weconclude thatpartialandtotalhemisphericdisconnectionsrevealoppositepatternsofhemisphericasymmetryin auditory,visualandaudio–visualemotionprocessing.Theseresultsarediscussedinthelightofthe right-hemispherehypothesisandthevalencehypothesis.
©2014ElsevierB.V.Allrightsreserved.
1. Introduction
Studiesonthecerebrallateralizationofemotionalprocessing
haveshownvariablepatternsofresults,andtheaspectof
hemi-spheric asymmetry in this field still remains controversial [1].
∗ Correspondingauthor.Tel.:+398713554216;fax:+3987135542163. E-mailaddress:giulia.prete@unich.it(G.Prete).
According to the right-hemisphere hypothesis [2–4], a
right-hemisphericdominancewouldunderlieallaspectsofemotional
processing.Ontheotherhand,accordingtothevalence
hypoth-esis [5–7] a right-hemispheric superiority would underlie the
processingofnegativeemotions,whereasaleft-hemispheric
supe-rioritywouldunderlietheprocessingofpositiveemotions.
Hemisphericasymmetriesinperceptionhavebeenexploredby
meansofseveralparadigms.Intheauditorydomain,the
organiza-tionofcerebralauditorypathwaysmakesitpossibletoevaluatethe
http://dx.doi.org/10.1016/j.bbr.2014.06.034 0166-4328/©2014ElsevierB.V.Allrightsreserved.
contributionofeachhemispherebypresentingdifferentstimuliin
thetwoears(dichoticlistening).Exploitingthisfact,anumberof
studieshaveshownthatthepresentationofanacousticstimulusin
oneearleadstoahigheractivationinthecontralateralhemisphere
(e.g.,rightear/lefthemisphere)ratherthanintheipsilateral
hemi-sphere[8,9].Inparticular,thedichoticlisteningparadigmreveals
arightearadvantage(REA),indicatingaleft-hemispheric
superi-orityinlinguisticprocessing[10,11],whichhasalsobeenshown
inecologicalcontexts[12].TheREAseemstobeattributableto
theinvolvementofthecorpuscallosum(CC)andtheauditory
cor-tex,besidesattentionalfactors(see[13]forareview).Moreover,
dichoticlisteninghasbeenusedtoinvestigatethelateralizationof
emotionalprocessingintheauditoryverbalandnonverbaldomains
[14].For example,Erhanandcolleagues[15] askedparticipants
tocategorize emotional prosody of dichoticallypresented
non-sensesyllablesashavingpositiveornegativeintonation,andthey
foundaleftearadvantage(LEA),eveniftheyunderlinedan
oppo-siteelectrophysiologicalcorrelate,namelyahigheramplitudeof
theN100component in theleftrather than inthe right
hemi-sphere.Theseauthorsproposedthatsuchapatternofevent-related
potentialsreflectsphoneticanalysisbutthatemotionalevaluation
isprocessedintherighthemisphere,thussupportingthe
right-hemispherehypothesis.Ofnote,however,Erhanandcolleagues
pointedoutthattheLEAwasstrongerfornegativethanforpositive
emotions([15],seealso[72]).Ontheotherhand,HerreroandHillix
[16]foundagenerallowerrecognitionscorefornegativethan
pos-itiveemotionalintonationsentences,andasignificantinteraction
betweenthepresentationearandtheemotionalvalenceofstimuli,
withaspecificloweringofscoresforthenegativeemotional
sen-tencespresentedintherightear.Schepmanetal.[17]haverecently
confirmedthispatternofresults,providingfurthersupportforthe
valencehypothesis.
Other controversial results were also obtained in EEG and
neuroimagingstudiesinwhichdifferentparadigmsthandichotic
listeningwereused.Recordingevent-relatedpotentialsandskin
conductance,Meyersand Smith[18] didnotfindasymmetryin
nonverbalaffectivestimuliprocessing.Nevertheless,inafunctional
magneticresonanceimagingstudy,Wildgruberandcolleagues[19]
founda strongeractivationoftherighthemisphereforacoustic
stimuliwithbothpositiveandnegativevalence,thussupporting
theright-hemispherehypothesis.
Cerebral lateralization has also been largely studied in the
domain of visual perception. Specifically, a paradigm used to
investigatecerebralasymmetriesinfaceprocessingisthatofthe
chimericfaces[2],thatarecreatedbyjuxtaposingtheleftandright
halvesof twodistinct faces.Studiesthat madeuseof chimeric
facesshowedthattherighthemisphereismorespecializedforface
processingthanthelefthemisphere[20].Alsointhiscontext,
how-ever,contrastingresultshavebeenobtainedasregardsemotion
processing.Presentingchimericemotionalfaces,Drebingand
col-leagues[21]providedsupportfortheright-hemispherehypothesis
[21].KillgoreandYurgelun-Todd[22],onthebasisofanfMRIstudy,
concludedthat the valence and theright-hemisphere
hypothe-sisarenotmutuallyexclusive,buttheyshouldbeconsideredas
differentpossibilitiestounderstandfacialemotionprocessing.A
similarlyunclearpatternofresultshasbeenachievedbyexploiting
bilateralpresentations oftwoemotionalfacesorunilateral
pre-sentationsofoneface,providingevidenceinsupportforboththe
right-hemispherehypothesis[23,24]andthevalencehypothesis
[25–27].
Withregardtoaudio–visualintegration,animportantquestion
iswhetherthefusionofmultisensoryinputsleadstoa
combina-tionoftheprocessingactivitiesinvolvedbyeachofthetwosensory
modalitiesconsideredinisolation,orwhethertheinformation
pre-sentedinonesensorymodalitypredominatesoverthatpresented
intheothermodality.Ofnote,anumberofstudiesshowedthat
multisensoryintegrationisautomaticandunintentional,although
otherstudiessuggestedadifferentpointofview(see [28]fora
review).Collignonandcolleagues[29]askedparticipantsto
clas-sifyvocalandvisualstimuliaccordingtotheiremotioncontent,
findingthatthecategorizationimprovedwhenvocaland visual
expressionswerecongruentand that,in theincongruent
condi-tions, participantsbased theirevaluationsmainlyon thevisual
component(visualcapture).Ontheotherhand,Petrinietal.[30]
foundtheoppositeresult,withtheacousticinformation
prevail-ingduringtheevaluationofincongruentaudio–visualemotional
stimuli(auditorycapture).Thus,itcouldbeconcludedthatthere
isareciprocalinfluenceduringauditoryandvisualprocessingof
emotionalinformationdependingoncongruence[31],butthe
pri-oritizationofonesensorymodalityovertheotherdoesnotseem
tofollowaclearrulewhenthetwomodalitiesconveyconflicting
contents.
Manystudiesfocusedonthecerebralcorrelatesofaudio–visual
integrationand showed thatdifferent cerebralareas are
impli-catedinthis process:for example,Kreifeltsandcolleagues[32]
foundthatthebehavioralimprovementduringthesimultaneous
presentationofemotionallycongruentbimodalstimulicorrelated
withanincreasedactivationinthebilateralposteriorsuperior
tem-poral gyrus([32]; see also[33], for a review) and in the right
thalamus;otherstudieshighlightedaleft-hemisphericactivation
during bimodal processing, in particular in the middle
tempo-ral gyrus[34,35]and in theposterior superior temporal sulcus
[36]. Jeongand colleagues[37] foundthat emotionally
congru-entaudio–visualpresentationsenhancedtheactivityinauditory
areas,whereasemotionallyincongruentpresentationsenhanced
theactivityinfacerecognitionareas,suchasthefusiformgyrus.
Ethoferandcolleagues[38]haverecentlyshowntheimportance
of the orbitofrontal cortex in themechanism of habituation to
facialexpressionsandprosody,whichhighlights theroleofthis
region as an important component of a system for emotional
processingoffacesandvoicesandasaneuralinterfaceamong
sen-soryareas.Finally,electrophysiologicaldatademonstratedanearly
audio–visualcrosstalkfollowingstimuluspresentation[39,34].
Anothersourceofinformationaboutaudio–visualneural
cor-relatescomesfrom studiesonneurological patients. Hayakawa
andcolleagues[40]showedthatapatientwithamygdalaand
hip-pocampuslesionscouldnotrecognizefearfromfacialexpressions,
butwasabletorecognizethemfromprosodicandverbalstimuli,
whereasapatientwithamoreextendedlesionbeyondthe
amyg-dalacouldnotrecognizefearexpressionsfromprosodicandverbal
stimuli,evenifhewasabletorecognizethemfromfacialstimuli
[40].
Although audio–visual integration has been largely
investi-gated, hemispheric lateralization in this field remains largely
unexplored,even more soin thecase of multisensory analysis
in emotionperception.One ofthepossiblesources ofevidence
consistsinstudyingsplit-brainpatients[41,42],individualswho
have undergone the surgical resection of the corpus callosum
(CC) as an extreme attemptto prevent thespread of epileptic
seizuresbetweenthe two hemispheres[43]. Importantly,
com-parisonsamongtheperformanceofpatientswhohaveundergone
different degrees of hemisphericdisconnection (total or partial
and,inthelattercase,indifferentregionsoftheCC)provideus
withararechancetostudyhemisphericcompetences[44].
Stud-ieswithcallosotomizedpatientsconfirmedtheright-hemispheric
superiorityinfaceprocessing[45],aswellastheleft-hemispheric
superiority(REA)indichoticlistening([46];see[47],forareview).
Howeverthehemisphericsuperiorityinemotionanalysisremains
controversialeven asregardssplit-brainpatients’results:Stone
etal.[48]showedthatbothdisconnectedhemispherescouldmatch
equally well facial expressions to emotion words, but the left
Fig.1. MidsagittalMRIofpatients.Leftpanel:A.P.’sbrain,showingtheanteriorsectionofthecorpuscallosum,whichsavesthesplenium.Rightpanel:D.D.V.’sbrain,showing thecompleteabsenceofcallosalfibers.
etal.[49],basedontheresultsofasplit-brainpatientwhowas
capabletodiscriminateemotionalfromneutralstimulipresented
inbothLVFandRVF,concludedthatemotionalprocessingcould
takeplaceineitherdisconnectedhemisphere,butonlytheright
hemisphereproducedanautonomicresponsetoemotionalstimuli
[49].Arecentstudyinwhichatotalsplit-brainpatientandan
ante-riorcallosotomizedpatientweretested,providedsupportforthe
righthemispherehypothesisinthecaseofbilateralpresentationof
faceswithahiddenemotionalcontent[24].AsreviewedbyGainotti
[50],theright-hemisphericsuperiorityinsubliminallypresented
emotionalcontentcouldbeexplainedbyasubcorticalasymmetry
inemotiondetection.
Theaimofthepresent studywastoinvestigatehemispheric
asymmetriesinaudio–visualintegrationandthewayinwhich
lat-eralizedvisualandacousticemotionalstimuliareprocessedbythe
twohemispheres. Accordingtopreviousevidenceonemotional
analysisinthevisualandacousticmodalities,onemightexpectthat
eithertheright-hemispherehypothesisorthevalencehypothesis
isapplicablealsototheaudio–visualdomain.
First of all, we expected a moderate hemispheric
asymme-try in emotion evaluation by healthy participants. Second, we
expectedamoreextremehemisphericlateralizationpatternina
totalsplit-brainpatientregardlessofthenatureofstimuli,dueto
thecompleteabsenceofreciprocalcallosalconnectionsbetween
the hemispheres. Finally, we expected that in a patient with
ananteriorcallosalsection,lateralizationwould appear weaker
comparedtothatofthetotalsplit-brainpatient,duetointact
con-nectionsbetweenposteriorcorticalareas,theposteriorpartofthe
CCbeingspared, butstrongercomparedtothatofhealthy
sub-jects,becauseofthecompletesegregationoftheanteriorareas.
However,wecouldnotpredictthedirectionofanylateralization,
becauseofthe mixedresultsavailable intheliterature in both
visualandacousticdomains, andtheabsenceof clearevidence
of cerebral asymmetry in multimodal integrationof emotional
stimuli.
2. Materialsandmethods
2.1. Participants
ApatientwithananteriorsectionoftheCC,apatientwitha
totalsectionoftheCC,and16healthyparticipantstookpartinthe
experiment.
A.P.isa47-year-oldman,whounderwentthesurgicalresection
ofalargeanteriorportionoftheCCtoreducethespreadofepileptic
seizures.Thesurgerywascarriedoutin1993anditleftintactonly
thesplenium(seeFig.1a).A.P.’spostoperativeIQwas87,as
mea-suredbymeansoftheWechsleradultintelligencescale(WAIS),
andhislateralityquotientwas+10,accordingtotheEdinburgh
HandednessInventory[51].
D.D.V.isa48-year-oldman,who,inordertopreventthespread
ofepilepticfoci,underwentthecompleteresectionofthecorpus
callosumthroughdifferentstages,thelastofwhichoccurredin
1994.Thesurgicalresectionleftintacttheanteriorcommissure(see
Fig.1b).D.D.V.’spostoperativeIQwas81,asassessedbytheWAIS,
andhislateralityquotientwas+100,accordingtotheEdinburgh
HandednessInventory[51].
Bothpatientshadnovisualimpairmentsorpsychiatric
symp-toms(furtherdetailsofthepatients’statusareprovidedby[52]).
TheyweretestedattheEpilepsyCenterofthePolytechnic
Univer-sityofMarche(Torrette,Ancona),duringapausebetweenroutine
neurologicalexaminations.
Thecontrolgroupwascomposedof16maleindividuals(age:
M=24.44; SD=1.35). According to self-report, all were
right-handed,hadnormal orcorrected-to-normalvision, andnoneof
themhadneurologicalorpsychiatrichistories.Theseparticipants
weretestedasvolunteersatthePsychobiologyLaboratoryofthe
UniversityofChieti.
Informedconsentwasobtainedfromallparticipantspriorto
thebeginningofthetaskandtheexperimentalprocedureswere
approvedbythelocalethicalcommittee.
2.2. Stimuli
Weusedchimericfacesasvisualstimulianddichotic
presenta-tionsasacousticstimuli.
Facialstimuliwerecreatedfromphotographscontainedinthe
Karolinska directed emotional faces [53], a database of female
andmalefaceswithbothneutralandemotionalexpressions.
Pho-tographsofafemalefaceinahappypose(HA)andinasadpose
(SA)wereselectedandconvertedintogray-scaleimages,
measur-ing5.2◦×6.6◦ofvisualangle(198×252pixel)atadistanceofabout
72cm.Fromtheseimages,hemifacecomponentswerecreated:the
twophotographswerecentrallydividedintotwohalves,inorderto
obtainoneleftsadhemiface,onerightsadhemiface,onelefthappy
hemiface,andonerighthappyhemiface.Chimericfaceswerethus
Fig.2. Anexampleofchimericface(HA/SA).
ofvisualstimuliwascomposedof4chimericfaces:HAleft
hemi-face/HArighthemiface,HAlefthemiface/SArighthemiface,SAleft
hemiface/HArighthemiface,SAlefthemiface/SArighthemiface.In
ordertoreducethesenseofstrangenesspossiblyduetochimeric
stimuli,thetwohalffaceswereseparatedbyathinwhitestripe
(width:.02◦ofvisualangle;seeFig.2).
Acousticstimuliwerecreatedbyrecordingconsonant–vowel
syllablespronouncedbyafemaleactresswithdifferentemotional
accent.Thesyllable/ba/wasrecordedwithtwodifferentemotional
intonations: happy(HA) and sad (SA). Stimuli were then
han-dledwithGoldWaveSoftwarev5.25(GoldWaveInc.,St.John’s,NL,
Canada).Theyweredigitized(16bit,samplingrate44,100Hz)and
presentedinadichoticparadigm,inwhichtheemotionalsyllable
waspresentedinoneearandwhitenoise(WN)wassimultaneously
presentedintheotherear.Acousticstimulilasted350ms,including
50msoflinearfade-inatthebeginningofeachstimulusand50ms
oflinearfade-outattheendofeachstimulus.Dichoticstimuliwere
deliveredbymeansofheadphones(PhilipsSHP5400):anemotional
syllableandwhitenoisewerepresentedintheoppositeears,with
acommononsetandacommondurationof350ms.Thefinalset
ofacousticpresentationswascomposedof4dichoticstimuli:HA
syllableintheleftear/WNintherightear,WNintheleftear/HA
syllableintherightear,SAsyllableintheleftear/WNintheright
ear,andWNintheleftear/SAsyllableintherightear.Wechoseto
avoidthesimultaneouspresentationofdifferentemotional
sylla-blesinthetwoearsinordertokeepthecomplexityofconflicting
informationbetweenvisualandauditoryinputasmanageableas
possibleforsubsequentstatisticalanalyses.
We presented happyand sad emotionalexpressions, onthe
basisofpreviousstudiesindicating thatthesetwoemotionsare
evaluated ashighly opposite in valence (positive and negative,
respectively),andarethuseasytodifferentiatefromeachother
[54]. We chose to use the 350ms presentation time to allow
patientstoeffectivelyprocessallstimulieveninthecaseofbimodal
(possiblyconflicting)conditions,inwhichthecognitiveloadcould
behigh.Wealsopreferredtousea relativelylongpresentation
timetomakesurethatthebimodalintegrationoccurred,giventhat
some electrophysiological data demonstrated that audio–visual
integrationmaytakeplaceonlyatabout180msafterstimulionset
[39]. Onthe otherhand,there isevidence oflateralized effects
obtainedwithlongpresentationtimeinboththeacoustic(e.g.,[55])
andthevisualdomain(e.g.,[56,57]).
2.3. Procedure
Participantswereadministeredfourdifferentsessionsinwhich
theywereaskedtoevaluatetheemotionalvalenceofstimuli,using
a5-pointLikertscale:from1=verysad,to5=veryhappy(1=very
sad;2=sad;3=neutral;4=happy;5=veryhappy),usingthe
com-puterkeyboard.
Inthefirstsession,onlyacousticstimuliwerepresented.The
4dichoticstimuliwerepresentedinrandomorder5timeseach,
constituting asetof 20acousticstimuli. Awhite screenlasting
500mswasfollowedbythepresentationofacentralfixationcross
for850ms.Afterafirstintervalof500msinwhichonlythecross
wasshown,thedichoticstimuluswaspresentedforadurationof
350ms,sothattheendoftheacousticinputcorrespondedtothe
endofthecrosspresentation.Then,thescreenwentblankuntilthe
responsewasgiven,andthenexttrialstarted(seeFig.3a).
Inthesecondsession,onlyvisualstimuliwerepresented.The
4chimericfaceswerepresentedinrandomorder5timeseach,
constitutingasetof20visualstimuli.Awhitescreenlasting500ms
wasfollowedbythepresentationofablackfixationcrossinthe
centerofthescreenfor500ms.Thestimuluswasthenpresented
inthecenter ofthescreenwithadurationof350ms.Then,the
screenwentblankuntiltheresponsewasgivenbytheparticipant,
andthenexttrialstarted(seeFig.3b).
Inthelasttwosessions,acousticandvisualstimuliwere
pre-sented together.Eachof thesesessions wereconstituted by80
stimuli,includingall16possiblecombinationsofthe4chimeric
facesand the4 dichoticpresentations, each combination being
repeated5timesinarandomorder.Thesetwosessionswere
simi-lartoeachother:awhitescreenwaspresentedfor500ms,followed
bythepresentationofablackfixationcrossinthecenterofthe
screenfor500ms.Thedisappearanceofthecrosscoincidedwith
thesimultaneousonsetofboththechimericfaceinthecenterof
thescreenandthedichoticstimulusintheearphones,bothlasting
350ms.Then,thescreenwentblankuntiltheresponsewasgiven,
andthenexttrialstarted(seeFig.3c).Inthefirstofthesetwo
ses-sions,participantswereaskedtoevaluatetheemotionalvalenceof
thevisualstimuli,ignoringtheacousticinput,whereas,inthelast
session,participantswereaskedtoevaluatetheemotionalvalence
oftheacousticstimuli,ignoringthevisualinput.
Inorder tospecifywhich modalityhadtobeattendedto,at
thebeginningofeachsessioninstructionswerepresentedonthe
computerscreen.Intheinstructionsitwasalsospecifiedthatthe
gazehadtobemaintainedatthecenterofthescreenforallthe
testingtime.Attheendofasession,participantswereallowedto
takeashortbreakbeforestartingthenextone.
Thetwopatientsgavetheirresponsesusingtherighthand.As
regardsthecontrolgroup,halfoftheparticipantsusedtheright
handandtheotherhalfusedthelefthand.Thewholetaskwas
controlledbyE-Primesoftware(PsychologySoftwareTools,Inc.,
Pittsburgh,PA)andlastedabout30min.
3. Results
StatisticalanalyseswerecarriedoutusingthesoftwareStatistica
8.0.550(StatSoft.Inc.,Tulsa,USA).Asregardscontrolgroupscores,
thedifferentconditionsineachofthe4sessionswerecompared
by meansofdifferentanalysis ofvariance (ANOVAs), using the
emotionjudgmentasthedependentvariable.PreliminaryANOVAs
Fig.3.Schematicrepresentationofatrialinsession1:dichoticstimuli(toppanel,ontheleft);insession2:chimericstimuli(toppanel,ontheright);andinsessions3and 4:bimodalpresentations,withbothdichoticandchimericstimuli(bottompanel).
between-subjectsfactor,butneitherthemaineffectofthis
fac-tornorinteractionsweresignificant.Thus,wecarried outthree
repeatedmeasuresANOVAs(oneforeachunimodalsession and
oneforthetwobimodalsessions).Post-hoccomparisonswere
car-riedoutbymeansofBonferronitestand correctedp-valuesare
reported.
Intheauditorysession,theANOVAwascarriedoutusing
emo-tionaltone(happyandsad)andpresentationear(leftandright)as
within-subjectfactors.Onlythemaineffectofemotionaltonewas
significant(F(1,15)=53.06,p<.001,2=.78),showingthathappy
syllables were evaluated ashappier than sad syllables (happy:
M=3.94±.14;sad:M=2.26±.10).
In the visual session, the ANOVA was carried out using
face as within-subject factor (happy/happy, sad/sad, happy/sad
andsad/happy).Thismaineffectwassignificant(F(3,45)=157.49,
p<.001, 2=.913): post-hoc comparisons showed that the
happy/happyface wasevaluated happier than all of the other
stimuli and that the sad/sad face was evaluated sadder than
all of the other stimuli (p<.001 for all comparisons; HA/HA:
M=4.74±.07;SA/SA:M=1.69±.12;HA/SA:M=2.90±.12;SA/HA:
M=2.72±.14).
Asregardsthetwobimodalsessions,theANOVAwascarried
outusingTargetmodality(visualandacoustic),face(happy/happy,
sad/sad,happy/sad and sad/happy),emotional tone(happy and
sad) and presentation ear (left and right) as within-subject
factors. The main effect of target modality approached
sta-tistical significance (F(1,15)=4.27, p=.056), visual stimuli being
evaluatedslightlymore positively(M=3.16±.07)thanauditory
stimuli (M=3.03±.08). The main effect of face wassignificant
(F(3,45)=36.05, p<.001 2=.71): post-hoc comparisons showed
thatthehappy/happyfacewasevaluatedhappierthanallofthe
other stimuli and that the sad/sad face was evaluated sadder
thanalloftheotherstimuli(p<.001forallcomparisons;HA/HA:
M=3.96±.1; SA/SA:M=2.38±.1; HA/SA:M=3.02±.09;SA/HA:
M=3.02±.08).Themaineffectofemotionaltone(F(1,15)=49.23,
p<.001,2=.77)showedthathappysyllableswereevaluatedas
happierthansadsyllables(HA:M=3.72±.07;SA:M=2.47±.06).
Themaineffectofpresentationearwasnotsignificant(F(1,15)=.55,
p=.47;left:M=3.09±.07;right:M=3.11±.07).
Asregardsthesignificantinteractionbetweentargetmodality
and face (F(3,45)=20.23, p<.001, 2=.57), post-hoc
compar-isons showed that when visual judgments were required, the
happy/happyfacereceivedahigherevaluationandthesad/sadface
receivedalowerevaluationcomparedtoalloftheotherconditions
(p<.001forallcomparisons),whereaswhenauditoryjudgments
wererequired,thehappy/happyfacewasassociatedtohigher
eval-uations than thesad/sadface (p<.001) and thesad/happy face
(p=.044).
Theinteractionbetweentargetmodalityandpresentationear
wassignificant(F(1,15)=6.34,p=.024,2=.30)andpost-hoc
com-parisonsshowedthatvisualjudgmentswerehigherthanauditory
judgments when syllables were presented both to the left ear
(visualmodality:M=3.17±.10;acousticmodality:M=3.00±.11;
p=.04),andtotherightear(visualmodality:M=3.15±.11;
acous-tic modality:M=3.06±.11;p=.002). Moreover,in theacoustic
modality,syllablespresentedtotherightearreceivedhigher
eval-uations than thosepresented tothe leftear (p=.036), whereas
evaluationsdidnotdifferaccordingtoauditorypresentationside
whenthetargetmodalitywasvisual.
Thethree-wayinteractionamongface,emotionaltoneand
pre-sentationear(F(3,45)=3.41, p=.025, 2=.18)wassignificant.To
betterclarifythisinteraction,twodifferentANOVAs were
com-puted,bysplittingthedataaccordingtopresentationearandusing
faceandemotionaltoneaswithin-subjectfactors.Asregardsthe
right-earpresentationcondition,asignificantinteractionbetween
faceandemotional tone(F(3,45)=4.60, p=.007,2=.23)showed
thatwhenthesadsyllablewaspresented,thesad/happyfacewas
judgedashappierthanthehappy/sadface(p=.047).Theinteraction
wasnotsignificantfortheleft-earpresentationcondition.
Inordertoevaluatetheeffectsofbimodalpresentations,mean
scoresobtainedinboththevisualandtheauditoryunimodal
Fig.4. 95%Confidenceintervalsofthecontrolgroup(lines)andpatientsmeans (A.P.:cross;D.D.V.:triangle)inthefirstsession:4dichoticstimuli.
sessions,usingaseriesofBonferronicorrectedt-tests.In
partic-ular,scoresrecordedinthebimodalsessioninwhichparticipants
wereaskedtojudgetheemotionalvalenceofthevisualstimuli
(session 3) were compared with scores recorded in the visual
session (session 2). The presentation of a happy tone to the
right ear (WN/HA) led to higher evaluations of the sad/happy
chimeric face (t(15)=−3.724, p=.032). In the same way, scores
recordedinthebimodalsessioninwhichparticipantswereasked
to judge the emotional valence of acoustic stimuli (session 4)
werecomparedwiththescoresrecordedintheauditorysession
(session1).Thepresentationof thesad/sadface ledtoa lower
evaluationof allacousticstimuli (HA/WN:t(15)=5.021,p=.002;
WN/HA:t(15)=3.764,p=.030;SA/WN:t(15)=3.68,p=.036;WN/SA:
t(15)=5.51,p<.001),whereasthepresentationofthehappy/happy
faceledtohigherevaluationsofthesadsyllablepresentedtoboth
theleft(SA/WN:t(15)=−4.69,p=.005)andtherightear(WN/SA:
t(15)=−5.397,p=.001).
Inordertocomparetheperformanceofthepatientsandthe
controlgroupineachsession,patients’meanswerecomparedwith
the95%confidenceintervalsofthecontrolgroupscores.
In session 1 (dichotic syllables), A.P.’smean wasabove the
cut-offofthe95%confidenceintervalsintheHA/WNcondition,
whereasD.D.V.’smeanswereaboveofthe95%confidenceintervals
inallconditions(seeFig.4).
Insession2(chimericfaces),A.P.’smeanswereabovethe
cut-offofthe95%confidenceintervalsinHA/HAandHA/SAconditions,
andtheywerebelowinSA/SAandSA/HAconditions.Inthissession,
D.D.V.’smeanswereabovethecut-offofthe95%confidence
inter-valsinHA/HAandSA/HAconditions,andtheywerebelowinSA/SA
andHA/SAconditions(seeFig.5).
Insession3(bimodalpresentationwithvisualevaluation),A.P.’s
meanswereabovethecut-offofthe95%confidenceintervalsin
allconditionsinwhichHA/HA andSA/SAfaceswerepresented,
regardlessof dichoticstimulation, and when HA/SAand SA/HA
faceswerepresentedtogetherwithSA/WNandWN/SAdichotic
stimuli. In this session, D.D.V.’s means were above the cut-off
ofthe95% confidenceintervals whentheHA/HA facewas
pre-sentedtogetherwithWN/HA,SA/WNandWN/SAstimuliandwhen
theSA/HAfacewaspresentedtogetherwithHA/WN,SA/WNand
WN/SAstimuli;theywerebelowthecut-offofthe95%confidence
intervalswhentheHA/HAfacewaspresentedtogetherwiththe
HA/WNdichoticstimulusandinalltheconditionsinwhichSA/SA
andHA/SAfaceswerepresented,regardlessofdichoticstimulation
(seeFig.6).
Fig.5.95%Confidenceintervalsofthecontrolgroup(lines)andpatientsmeans (A.P.:cross;D.D.V.:triangle)inthesecondsession:4chimericfaces.
Insession4(bimodalpresentationwithauditoryevaluation),
A.P.’smeanswereabovethecut-offofthe95%confidence
inter-valswhentheHA/WNdichoticstimuluswaspresentedtogether
withSA/SAandHA/SAfaces,whentheWN/SAdichoticstimulus
waspresentedtogetherwithSA/SAand SA/HAfaces,and in all
conditionsinwhichWN/HAandSA/WNstimuliwerepresented
togetherwithanychimericface.In this session,D.D.V.’s means
wereabovethecut-offofthe95%confidenceintervalswhenthe
HA/WN stimuluswaspresented togetherwiththe HA/HAface,
whentheWN/HAstimuluswaspresentedtogetherwithHA/HA
andSA/HAfaces,whentheSA/WNdichoticstimuluswaspresented
togetherwiththeSA/HAface,andwhentheWN/SAstimuluswas
presentedtogetherwithHA/HA,HA/SAandSA/HAfaces;theywere
below whentheHA/WNstimuluswaspresented togetherwith
bothSA/SAandHA/SAfaces,whentheWN/HAstimuluswas
pre-sentedtogetherwiththeHA/SAface,andwhentheSA/WNstimulus
waspresentedtogetherwiththeSA/SAface(seeFig.7).
4. Discussion
Theperformancesofthetwopatientswereverydifferentfrom
oneanother.Ingeneral,thetotalsplit-brainpatient(D.D.V.)showed
arightwardbias;moreover,hisevaluationsinbimodal
presenta-tionsweremainlybasedonvisualratherthanacousticstimuli,even
whenhewasexplicitlyrequiredtojudgetheauditoryinput.Onthe
otherhand,theresultsofthepartiallycallosotomizedpatient(A.P.)
largelyresembledthoseofthecontrolgroupandhedidnotshow
difficultiesinpayingattentiontoeithervisualoracousticstimuli,
whenrequired.Differentlyfromthecontrolgroup,however,A.P.
showedatrendforaleftwardbiasintheemotionalevaluationof
bothacousticandvisualstimulipresentedinisolation.This
pat-ternofresultsconfirmsaright-hemisphericsuperiorityinemotion
detection,alreadyknowninthevisualdomain(see[24],forsimilar
lateralizationresultsinthesamepatient),andaddsnewevidence
intheauditorydomain.
AsregardstheresultsofD.D.V.,intheauditorysessiontheyseem
tobeinlinewiththevalencehypothesis,giventhatheattributed
ahigherscoretohappysyllablespresentedtotherightthantothe
leftear,andatthesametimeheattributedalowerscoretosad
syllablespresentedtotheleftthantotherightear[5–7].However,
thispatternwasnotevidentintheotherconditions.In
particu-lar,withvisualpresentation,D.D.V.seemedtotallyincapableat
detectingemotionsexpressedbythelefthemiface:hisjudgments
werebasedsolelyontheexpressionoftherighthemiface.Atfirst
Fig.6.95%Confidenceintervalsofthecontrolgroup(lines)andpatientsmeans(A.P.:cross;D.D.V.:triangle)inthethirdsession,inwhichchimericfacesanddichoticstimuli werepresentedtogetheranditwasaskedtoevaluatethevisualstimuli:16bimodalconditions.
dominance,thatcouldbeascribedeithertoahemispheric
asymme-tryinemotionalfaceprocessingortoaleft-hemisphericdominance
duetotheuseoftherighthandforresponding.However,another
explanationcouldbefoundintheliteratureonsplit-brainpatients.
Infact,severalstudiescarriedoutwithsplit-brainpatientsshowed
–onlyfollowingtotalresection–asortofattentionaldeficitofthe
righthemisphere[58,59,24].Inthepresentstudy,theuseofthesole
righthandinprovidingresponses,makesitdifficulttoconcludeif
D.D.V.showedaspatialneglectorless,however,testingthesame
split-brainpatient(D.D.V.),Hausmannandcolleagues[58]founda
rightwardbiaswhenD.D.V.carriedoutalinebisectiontaskusing
eithertheleftortherighthand;Corballisandcolleagues[59,60]
describedthesamekindofbiasinD.D.V.leadingtheauthorsto
concludethatD.D.V.showsasortofspatialhemineglect.A
cru-cialpointisthattheresultsofD.D.V.areincontrastwiththoseof
otherpatientswithpartial(eitheranteriororposterior)
calloso-tomy,whodonotshowhemineglect.Corballisandcolleagues[59]
proposedthatthespatialneglectofD.D.V.,causedbythecomplete
Fig.7.95%Confidenceintervalsofthecontrolgroup(lines)andpatientsmeans(A.P.:cross;D.D.V.:triangle)inthefourthsession,inwhichchimericfacesanddichotic stimuliwerepresentedtogetheranditwasaskedtoevaluatetheauditorystimuli:16bimodalconditions.
absenceofcallosalfibers,isduetoafailuretoshiftattentionfrom
therighthemifieldtothelefthemifield,andtheysuggestedthe
possibilitytotestthesamepatientwithouttheuseofthecentral
fixationcross,inordertoavoidtheneedtoshiftattentionfromthe
centertothesideofthescreen.Inthepresentstudythisproblem
wasinsomewaysidestepped,bymeansofshowingchimericfaces
inthecenterofthescreen.Nevertheless,thepresentresultsseem
toconfirmthepresenceofhemineglectinpatientD.D.V.Moreover,
weaddednewdata,testingthepatientwithacousticstimuli:from
thepresentresultswecanconcludethatthespatialneglectofD.D.V.
isnotapplicabletotheauditorydomain,differentlyfrompatients
whosufferfromhemineglectafteraunilateralcerebrallesion[61],
butitseemstobeconfinedtothevisualdomain.Intheauditory
domain,aconsonant-voweldichoticparadigmcarriedoutwith4
split-brainpatients[62]showedthattheREAwasequivalentfor
therightandthelefthandresponding.Overall,theexplanationof
ourresultsasduetotheuseoftherighthandwouldnotbevalid
intheauditorysession,inwhichD.D.V.didnotshowtherightward
bias,evenifheusedtherighthandonly.
Duringthebimodalpresentation,acousticstimuliwere
substan-tiallyignoredbyD.D.V.,whobasedhisresponsesontheright
hemi-face:giventhatD.D.V.couldsuccessfullycarryoutthedichotictask,
hedisregardedacousticstimulionlyinthecaseinwhichtheywere
presentedtogetherwithvisualstimuli.Inotherwords,thedichotic
presentationalonehighlightedthevalidityofthevalence
hypothe-sis,withopposite-valenceemotionsbeingprocessedbetterbythe
twohemispheres,whereasthesimultaneousaudio–visual
presen-tationshowedasupremacyofthevisualstimuliovershadowing
theacousticstimuli(visualcapture).Thiswasofcoursetruewhen
D.D.V.wasrequiredtoevaluatevisualstimuli,but,importantly,also
whenrequiredtoevaluateacousticstimuli.
Thissetofresultsshowsamultifacetedpicture.Whereas
Cor-ballisandcolleagues[59]concludedthattheattentionaldeficitof
D.D.V.isattributabletoadeficitin shiftingattention,anability
involvingthe ventralattentional system,and that it could
dis-appearifD.D.V.canbasehisresponsesonthedorsalattentional
system,ourresultsseemtosupportanotherperspective:themain
deficitofthepatientdoesnotseemtoresideinattentional
shif-ting,butin hisattentionalbiastowardtherightvisualfield. In
fact,chimericfaceswerepresentedcentrally,thusnotrequiring
gazeorientingorattentionalshift,butnonethelessD.D.V.showed
arightwardbias.Moreover,amongtheperceptualmodalitieswe
tested,thevisualmodality,butnottheauditorymodality,revealed
aspatialhemineglect.Inconclusion,theresultsofthetotal
split-brainpatientprovidedsupportforthevalencehypothesisinthe
auditorydomain,showedahemineglectinthevisualdomain,and
revealedastrongvisualcapture,thusconfirmingthehemineglect,
inaudio–visualprocessing.
Theresultsoftheanteriorsplit-brainpatient,A.P.,were
differ-entfromthoseofD.D.V.inallsessions.Indichoticpresentations,
A.P.’sevaluationsseemtosupporttherighthemisphere
hypothe-sis:happyandsadsyllableswereevaluatedashappierandsadder,
respectively,whenpresentedintheleftear(righthemisphere)than
intherightear(lefthemisphere),supportingtheright-hemispheric
dominanceinemotionalprocessingofbothpositiveandnegative
expressions.Theresultsinthevisualmodalityalsoprovidesupport
fortherighthemispherehypothesis:thehappy/sadchimericface
wasevaluatedashappierbyA.P.thanbythecontrolgroup,andthe
sad/happychimericfacewasevaluatedassadderbyA.P.thanby
thecontrolgroup.Thispatternshowsthatinthepartialsplit-brain
patient,theright-hemispheric dominanceforboth positive and
negativeemotionsmightbeevenmoreevidentthaninthecontrol
group.Inaudio–visualpresentations,A.P.didnotshow
difficul-tiesinevaluatingeithervisualoracousticstimuli.However,inthe
bimodalsessioninwhichvisualevaluationswererequired,A.P.’s
resultsdidnotsupporttherighthemispherehypothesis,butthey
seemedtobeinlinewiththevalencehypothesis:theevaluationsof
thechimericfaceswerelowerwhenthesadsyllablewaspresented
totheleftear(righthemisphere)andhigherwhenthehappy
sylla-blewaspresentedtotherightear(lefthemisphere).Inthebimodal
conditioninwhichauditoryevaluationswererequired,theresults
ofA.P. showedthat whentheemotionalsyllables,regardlessof
theirvalence,werepresentedtotheleftear(righthemisphere),
theyledtoagreaterweightofthe(hemi)facialexpressionshown
totheleft(thus,totherighthemisphere),withlowerscoresforthe
chimericsad/happythanhappy/sadface;whentheemotional
syl-lableswerepresentedtotherightear(lefthemisphere),theyledto
agreaterweightofthe(hemi)facialexpressionshowntotheright
(thus,tothelefthemisphere),withlowerscoresforthechimeric
happy/sadthansad/happyface.Theseresultssuggestthatwhen
auditoryevaluationswererequired,thehemispherecontralateral
totheearpresentedwiththesyllablewasmoreactivated,which
ledtoagreatersalienceofthecontralateralhemiface.Toconclude,
theresultsoftheanteriorcallosotomizedpatientprovidesupport
fortherighthemispherehypothesisonlywithunimodal
stimula-tion.ItisimportanttonotethatthedifferencebetweenD.D.V.and
A.P.isthepresenceofthespleniuminA.P.,whohoweverlacksall
theotherportionsoftheCC.Bymeansofdiffusion-weightedtensor
magneticresonanceimagingandprobabilistictractography,Beer
etal.[63]haverecentlyshownthepresenceofdirectconnections
betweenvisualandauditorycorticeswithineachhemisphereand
thatwhitematterprojectionsfrombothvisualandauditoryareas
crosshemispheresintheposteriorportionoftheCC,withauditory
andvisualinformationpassingthroughthesuperiorandinferior
splenium,respectively.Thisanatomicalevidencelendssupportto
theresultthattheperformanceofA.P.wasverysimilartothatof
thecontrolgroup,becauseinbothcasesaudio–visualinformation
maybeexchangedbetweenhemispherestroughthefibersofthe
splenium.However,somedifferenceexistsbetweenA.P.andthe
controlgroup,suggestingthatothercallosalregionsareimplicated
inthistask.
Thecontrolgroupdidnotshowhemisphericasymmetriesin
unimodalpresentations. Asreportedabove, weexpecteda
pat-ternof lateralizationin favor ofeither thevalence or theright
hemispherehypothesis.Theabsenceofevidenceinanydirection
in visualand auditory sessionscould beattributed tothelong
presentationtimeused.Aswespecifiedabove,wechoselonger
pre-sentationtimescomparedtotheclassicalrangeoftachistoscopic
presentation(around150ms)toensurestimulusprocessingbythe
patients.However,asignofhemisphericlateralizationisevident
intheinteractionbetweentargetmodalityandpresentationear:in
fact,whenanauditoryjudgmentwasrequired,syllablespresented
totherightearreceivedhigherevaluationsthansyllablespresented
totheleftear.Thisresultcouldbeinterpretedinthedirectionof
thevalencehypothesis:whentherighthemisphereisactivated
by the presentationof a syllable, auditoryjudgments decrease
possibly because of the right-hemispheric sensitivity for
nega-tiveemotions.Similarly,whenauditoryevaluationswererequired,
thehappy/happyfacewasjudgedashappierthanthesad/happy
face,butnotthanthehappy/sadface.Again,thisresultcould
sug-gestthattherighthemisphereismoresensitivethantheleftin
detectingthesadhemiface.Ontheotherhand,directcomparisons
betweenunimodalandbimodalsessionspointinthesame
direc-tion:thesad/happychimericfacewasjudgedashappierwhenit
waspresentedtogetherwiththehappysyllabletotherightear
(lefthemisphere),whereasnodifferenceswererecordedwhenthe
samesyllablewaspresentedtotheleftear(righthemisphere):in
accordancewiththevalencehypothesis,thehigheractivationof
thelefthemisphere,moreinvolvedinpositiveemotionprocessing,
couldhaveledtojudgethefaceashappier.Theabsenceofother
evidenceinsupportofthevalencehypothesisinhealthy
explainthepatients’moreasymmetricperformances.In fact,in
theseconditions A.P.based his ratingsontheleftward stimuli.
Probably,inthecaseofunimodalstimulation,afterthebilateral
exchange of perceptual analysis, which can occur through the
intact splenium of the patient, the outputof each hemisphere
couldbeprojectedtowardthefrontalareas(byintrahemispheric
fibers),where theabsenceofanterior interhemispheric
connec-tionspreventsthebalancebetweenhemispheres,leadingtothe
right-hemisphericsuperiorityinemotionalprocessing.This
possi-bilityisinaccordancewiththe‘modifiedvalencehypothesis’(MVH,
[64,65]):theclassicalhemisphericsuperiorityinaspecificvalence
emotionalanalysis(valencehypothesis)woulddependonthe
pre-frontalspecializationinpositiveandnegativeemotionalcontent
byeachhemisphere,whiletheposteriorregionwouldshowthe
right-hemisphericsuperiorityinallemotionalprocessing.Despite
theMVHdidnotreceivegreatconsideration,recentstudies
sup-portitsvalidity.Forexample,Stefanicsetal. [66]haverecently
foundsupportfortheMVH,recordingERPsduringtheprocessingof
unattendedfacialemotions,withearlycomponentssupportingthe
righthemispherehypothesis,andlatelateralizedcomponents
sup-portingthevalencehypothesis.ConsideringthatA.P.’sfrontallobes
weredisconnected,theMVHcouldexplainhisperformance.
How-ever,intheunimodalacousticcondition,theperformanceofD.D.V.
providedsupportforthevalencehypothesis.Fromthispatternof
results,wecansupposethatinthecaseoftotalinterhemispheric
disconnection,eachhemisphereshowsitssuperiorityinaspecific
emotionaldomain.Alsothispatternofresultcouldbeviewedin
accordancewiththeMVH:thecompletecallosalsectioninD.D.V.
doesnotallowanexchangebetweenthehemispheres,thusthe
relativedominanceofeachhemispherecouldemerge.Fromthis
perspective,thefrontalareasofD.D.V.receivea‘specialized’
out-putfromtheposteriorareasinwhichavalence-specificprocessing
wascarriedout.Thereafter,asregardsthetwomainhypotheseson
lateralizedemotionprocessing,wecanspeculatethattheyareboth
true,withtherighthemispherehypothesissupportedinthecase
ofpartialhemisphericconnections(A.P.)andthevalence
hypoth-esissupportedinthecaseofhemisphericindependence(D.D.V.).
Moreover,inbimodalsessions,theincreasedweightofcognitive
load–duetothesimultaneousstimulationsofbothhemispheres–
reducestheright-hemisphericsuperiority,supportinginanycase
thevalencehypothesis, exceptfor theperformanceofthe
split-brainpatient,whichweattributetoanattentionalbiasratherto
anasymmetricemotionalprocessing.Finally,thereistoconsider
thatthemeanageofthecontrolgroupislowerthanthatofthe
patients.However,itiswellknownthatastrongdifferenceexistin
callosalmorphometryconcerningbothsexandage[67].Theeffect
ofsexwascontrolledinthisstudy,testingallmaleparticipants.As
regardstheeffectofage,callosalmorphometricchangesareshown
especiallybeforereachingadulthood[68],whenthecallosalfibers
arenotcompletelymyelinated,butanumberofstudieslackedin
tiveemotion processing arefound in (i)bimodal presentations
inthecontrolgroup(connectedhemispheres),(ii)bimodal
pre-sentationsinA.P.(anteriorlydisconnectedhemispheres),and(iii)
acousticpresentationinD.D.V.(totallydisconnectedhemisphere).
Asregardsbimodalpresentations,wefoundastrongvisualcapture
inthecaseoftotallydisconnectedhemispheres.Importantly,when
visualstimuli werepresented (alone or together withacoustic
stimuli), only the total split-brain patient showed a
predomi-nantroleofthelefthemisphere,probablyduetoanattentional
bias,ratherthananasymmetricemotionalprocessing,whichwas
notpresentinauditoryprocessing.Thedebateonthevalidityof
theright hemisphere/valencehypothesis remains controversial,
butthepresentstudyaddsevidenceinsupportofboth theories
dependingonthetask,andsuggeststhatthevalencehypothesis
ismoreabletoaccountforresultsasthecognitiveloadbecomes
heavier.
Acknowledgments
WethankProfessorGabrielePolonaraforprovidinguswiththe
MRIimagesofthepatients.WealsothankverymuchD.D.V.and
A.P.fortheirwillingnesstocollaborateinthisstudy.
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