Processing of emotional vocalizations in bilateral inferior frontal cortex

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Article

Reference

Processing of emotional vocalizations in bilateral inferior frontal cortex

FRÜHHOLZ, Sascha, GRANDJEAN, Didier Maurice

Abstract

A current view proposes that the right inferior frontal cortex (IFC) is particularly responsible for attentive decoding and cognitive evaluation of emotional cues in human vocalizations.

Although some studies seem to support this view, an exhaustive review of all recent imaging studies points to an important functional role of both the right and the left IFC in processing vocal emotions. Second, besides a supposed predominant role of the IFC for an attentive processing and evaluation of emotional voices in IFC, these recent studies also point to a possible role of the IFC in preattentive and implicit processing of vocal emotions. The studies specifically provide evidence that both the right and the left IFC show a similar anterior-to-posterior gradient of functional activity in response to emotional vocalizations. This bilateral IFC gradient depends both on the nature or medium of emotional vocalizations (emotional prosody versus nonverbal expressions) and on the level of attentive processing (explicit versus implicit processing), closely resembling the distribution of terminal regions of distinct auditory pathways, which [...]

FRÜHHOLZ, Sascha, GRANDJEAN, Didier Maurice. Processing of emotional vocalizations in bilateral inferior frontal cortex. Neuroscience and Biobehavioral Reviews , 2013, vol. 37, no.

10 Pt 2, p. 2847-2855

DOI : 10.1016/j.neubiorev.2013.10.007 PMID : 24161466

Available at:

http://archive-ouverte.unige.ch/unige:84143

Disclaimer: layout of this document may differ from the published version.

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ContentslistsavailableatScienceDirect

Neuroscience and Biobehavioral Reviews

j o ur na l ho me p a g e :w w w . e l s e v i e r . c o m / l o c a t e / n e u b i o r e v

Review

Processing of emotional vocalizations in bilateral inferior frontal cortex

Sascha Frühholz

^a,b,∗

, Didier Grandjean

^a,b

aNeuroscienceofEmotionandAffectiveDynamicsLab,DepartmentofPsychology,UniversityofGeneva,Geneva,Switzerland

bSwissCenterforAffectiveSciences,UniversityofGeneva,Geneva,Switzerland

a r t i c l e i n f o

Articlehistory:

Received10April2013

Receivedinrevisedform9August2013 Accepted14October2013

Keywords:

Voice

Emotionalvocalizations Prosody

Inferiorfrontalcortex fMRI

a b s t r a c t

Acurrentviewproposesthattherightinferiorfrontalcortex(IFC)isparticularlyresponsibleforattentive decodingandcognitiveevaluationofemotionalcuesinhumanvocalizations.Althoughsomestudies seemtosupportthisview,anexhaustivereviewofallrecentimagingstudiespointstoanimportant functionalroleofboththerightandtheleftIFCinprocessingvocalemotions.Second,besidesasupposed predominantroleoftheIFCforanattentiveprocessingandevaluationofemotionalvoicesinIFC,these recentstudiesalsopointtoapossibleroleoftheIFCinpreattentiveandimplicitprocessingofvocal emotions.ThestudiesspeciﬁcallyprovideevidencethatboththerightandtheleftIFCshowasimilar anterior-to-posteriorgradientoffunctionalactivityinresponsetoemotionalvocalizations.Thisbilateral IFCgradientdependsbothonthenatureormediumofemotionalvocalizations(emotionalprosodyversus nonverbalexpressions)andonthelevelofattentiveprocessing(explicitversusimplicitprocessing), closelyresemblingthedistributionofterminalregionsofdistinctauditorypathways,whichprovide eitherglobalordynamicacousticinformation.Herewesuggestafunctionaldistributioninwhichseveral IFCsubregionsprocessdifferentacousticinformationconveyedbyemotionalvocalizations.Althoughthe rostro-ventralIFCmightcategorizeemotionalvocalizations,thecaudo-dorsalIFCmightbespeciﬁcally sensitivetotheirtemporalfeatures.

Contents

1. Introduction... 2848

2. AnatomyandfunctionsofthelateralIFC... 2849

3. AgeneralfunctionalroleoftheIFC... 2850

4. OriginsoftheIFCsensitivitytovocalintonations... 2850

5. ThefunctionalroleoftheIFCinprocessingemotionalvocalizations... 2851

6. LeftandrightIFCsubregionsforthedecodingofemotionalvocalizations... 2852

6.1. Attentionalfocus:attentiveandpreattentiveprocessingofemotionalvocalizations... 2852

6.2. Themediumofvocalexpressions ... 2852

7. Conclusionsandfuturedirections... 2853

Acknowledgments... 2854

AppendixA. Supplementarydata... 2854

References... 2854

∗Correspondingauthorat:UniversityofGeneva,SwissCenterforAffectiveSciences,7RuedesBattoirs,CH-1205Geneva,Switzerland.Tel.:+41223799688.

E-mailaddresses:sascha.fruehholz@unige.ch,fruehholz@gmail.com(S.Frühholz).

http://dx.doi.org/10.1016/j.neubiorev.2013.10.007

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2848 S.Frühholz,D.Grandjean/NeuroscienceandBiobehavioralReviews37(2013)2847–2855 1. Introduction

Thelateralinferiorfrontalcortex(IFC)mainlyconsistsofthe inferiorfrontalgyrus(IFG)andthefrontaloperculum(fOP).Besides several functions related to executive processes that generally regulateothercognitivefunctions,activityintheIFCisstrongly involved in the processing of humanvocal utterances, suchas speech(Friederici,2012).TheIFCisalsoconsistentlyinvolvedinthe processingofnonverbalandspeech-basedvocalintonations,such asspeechprosody(Frühholzetal.,2012;FrühholzandGrandjean, 2012;Schirmer and Kotz,2006)(seeFig. 1).Linguistic prosody referstothesuprasegmentalintonationalcontourduringverbal utterancesandseemstomainlyactivatetherightIFC(Bryan,1989;

FriedericiandAlter,2004).Similarly,emotionalprosody,thatis,the emotionallyinfluencedtoneofavoice(BanseandScherer,1996), elicitsstrong and replicable right IFCactivation (e.g. Buchanan et al.,2000; Georgeet al., 1996; Wildgruber et al.,2004).This findingsupportsearlyproposalsofthecriticalinvolvementofthe righthemisphereinprosodyprocessingingeneral(Ross,1981)and specificallyemotionalprosody(RossandMonnot,2008,2011;Ross etal.,1997;vanLancker,1980).Thus,comparedwiththepredomi- nantsyntacto-semanticprocessingintheleftIFC(Friederici,2012), therightIFCisthoughttobestronglyinvolvedintheprocessing ofthedynamicsofvocalemotionalintonations.Thishasalsobeen recentlyputforwardasthefinalstageofamulti-stagemodelof emotionalprosodyprocessing(SchirmerandKotz,2006),specif- icallyservingtheexplicitandcognitivecontrolledevaluationof vocallyexpressedemotions(Brucketal.,2011;Wildgruberetal., 2009).

However,therightIFCseemsnottohavea soleand unique roleintheprocessingofprosody,especiallyemotional prosody.

First,manyrecentstudiesfoundbilateral(Beaucousinetal.,2007;

Ethoferetal.,2006;Frühholzetal.,2012;Kotzetal.,2003;Morris etal.,1999)oreven speciﬁcleftIFCactivity(Bachet al.,2008;

Fecteauetal.,2005; Mitchell,2006;Wildgruber etal.,2004)in responsetoemotionalprosodyinseveralsubregionsoftheIFC(see

Fig.2).Thisobservationisalsosupportedbyrecentclinicalstud- iesshowingimpairedvocalemotionprocessinginpatientswith leftIFCbrainlesionsorbrainatrophy(Adolphsetal.,2002;Rohrer etal.,2012).Asecondsurprisingﬁndingisthatevenvoicemelody innonverbalvocalexpressions(Fig.1A,upperpanel),devoidof anylanguage-likesyntacto-semanticfeatures,canactivatesome subregions ofthe leftIFClanguageareas (Fecteau etal., 2005).

Althoughnonverbalexpressionsaredifferentbecausetheyarenot superimposedonspeechorspeech-likeutterancesand areusu- allylesstemporarilyextended,theymightﬁgureasprecursorsto emotionalintonatedspeech(ArnoldandZuberbuhler,2006;Belin etal.,2008a;Hauser,1997;seealsoSection4).Accordingly,non- verbalexpressionshavemanyacousticfeaturesincommonwith emotionalprosody (BanseandScherer,1996;Patel etal.,2011;

Sauteretal.,2010),fromwhichlistenersinfertheemotionalstate ofthespeaker.TheleftIFCthusmightalsodecodeemotionalcues fromnonspeechvocalizations,indicating thatleftIFCactivityis notexclusivetosyntacto-semanticspeechprocessing,butserves moregeneralfunctionsduringtheprocessingofhumanutterances.

Finally,althoughtheIFChasbeenproposedtobeinvolvedinthe explicitdecodingofemotionalprosodywhenattentionisdirected totheemotionalcuesinvoices,IFCactivityhasalsobeenfound whenattentionis directedaway fromemotionalcuesin voices (Belin et al.,2008a; Fecteauet al.,2005; Frühholz etal., 2012;

Morrisetal.,1999;Wildgruberetal.,2004,2005)orduringpassive listening(Mitchelletal.,2003).Thiscontradictssomeproposals thattheIFCispredominantlyinvolvedintheexplicitevaluationof emotionalvoicesorwhenattentionisdirectlyfocusedontheemo- tionalvalueofvoices(Brucketal.,2011;SchirmerandKotz,2006;

Wildgruberetal.,2009).

Boththe left and the right IFCare thus considerably active inresponse toemotional vocalizationsacrossdifferentlevelsof attentionalprocessing,allowingnoclearhemisphericdistinction.

However,therecentliteratureontheneuralbasisofvocalemo- tiondecodingseemstoshowthatinsteadofaleftandrightIFC distinction, arostral-to-caudal distinction existsin thebilateral

Fig.1.(A)Studiesinvestigatingtheprocessingofemotionalcuesfromvoicesuseeithernonverbalvocalexpression(upperrow;theexamplesshowsspectrogramofstimuli takenfromtheMAVdatabase;seeBelinetal.,2008b)oremotionalintonationssuperimposedonspeechorspeech-likeutterances,referredtoasemotionalprosody(lower row;spectrogramsonthepseudo-word“belam”;seeFrühholzetal.,2012).Althoughnonverbalexpressionsandemotionalprosodyaredifferentinnature,theyshare commonacousticfeatures(suchaspitchorintensitylevelandvariation),fromwhichlistenersdecodetheemotionalmeaningofvocalizations.(B)Besidesthedifferences relatedtothestimulusmaterial,studiesoftenusedifferenttaskstomanipulatethefocusofattentionduringtheprocessingofemotionalvocalizations.Thelattercanbe experimentallymanipulatedsuchthatemotionalcuesinvoicescanbepresentedinsideoroutsidethefocusofattention.Whenemotionalvoicesarepresentedinside thefocusofattention(whichwerefertoasexplicitattentionortask),participantshavetomakeadecisionontheemotionalvalenceofvoices(asshowninA),allowing acognitivelycontrolledprocessingofemotionalcuesinvocalizations.Thepresentationofemotionalvoicesoutsidethefocusofattention(whichwerefertoasimplicit attention)requires,forexample,thatparticipantsfocusonthegenderofthespeaker(leftpanel)(e.g.Frühholzetal.,2012),orthattheydirectspatialattentiontoanother sourceawayfromthespatiallocationofemotionalvoices(e.g.Grandjeanetal.,2005)(rightpanel,upperpart;thelowerpartshowsattentiontowardthespatiallocationof emotionalvoices).Duringanimplicitattentionalfocusortask,itisassumedthattheemotionaltoneofavoiceisstillprocessedonanimplicitlevel.

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Fig.2.Activationfociintheinferiorfrontalcortex(IFC)(A)accordingtotheattentionalfocus(explicitattentionortask(red),implicitattentionortask(green),passive listening(blue))and(B)accordingtothemediumofvocalexpressions(nonverbal,emotionalprosody).Foractivationfociaccordingtoattentionalfocus,oneactivationfocus inrightinferiorBA47wasfoundduringpassivelisteningtoemotionalvocalizations(triangle;Mitchelletal.,2003).BlackdotsinAindicatepeakactivationstakenfrom studiesforwhichgeneralIFCactivitywasfoundindependentofattentionalfocus.PeakactivationfociarerenderedonthehumanPALSatlasasimplementedintheCARET atlas(VanEssenetal.,2001).Weincludedonlyactivationfoci,whichwerederivedfromaclearfunctionalcomparisonbetweenexperimentalconditionsthatallowedaclear functionalspeciﬁcation;activationfociresultingfromacomparisonagainstabaselineconditionwithnoauditorystimulationwerenotincluded(seeSupplementS1forthe studiesincludedhere).ThewhitedottedlinesandthewhitenumbersdenoteBrodmannareas(BA)takenfromthesameCARETatlas.Abbreviations:cscentralsulcus,fop frontaloperculum,insinsula.(Forinterpretationofthereferencestocolorinthisﬁgurelegend,thereaderisreferredtothewebversionofthearticle.)

IFC.Basedonthenatureofvocalintonations(emotionalprosody versusnonverbalexpressions),aswellasontheattentionallevelin theprocessingofvocalizations,thisdistinctionresemblesarecent notionputforwardfortheleftIFCinspeechprocessing(Hagoort, 2005).TheIFCis nota uniquebrainarea, butrather comprises severalsubregions accordingtocytoarchitectonicand especially connectivity-basedparcellations(seeFig.3).Thisrostral-to-caudal distinctionintheIFCcloselyfollowstheterminationareasofthe dorsalandventralauditorypathwaysoriginatingindifferentparts ofthebilateralsuperiortemporalgyrus(STG).Accordingly,wepro- posearostro-ventraltocaudo-dorsaldistinctioninboththeleftand therightIFC,whichlikelysupportsdifferentfunctionalrolesduring theprocessingofemotionalvocalizationsbasedondifferentacous- tical information provided bydifferentauditorypathways. This proposalisoutlinedindetailhere,alongwithrecentevidencefor it.Webeginwithageneralanatomicalandfunctionaldescription oftheIFC.

2. AnatomyandfunctionsofthelateralIFC

The lateral IFC is primarily composed of the inferior gyrus consistingofBrodmannareas(BA)47/12,45,and44fromanterior

toposterior.VentrallytoBA44and45liesthefOP,primarilycov- eredbyBA47/12(Fig.3).ThesubdivisionoftheIFCintodifferent subregions is based on cytoarchitectonic (Amunts et al., 1999;

Petrides and Pandya,2002) and connectivity-based approaches (Anwander et al., 2007; Petrides and Pandya, 2002) and has revealed homologous areas in the nonhuman and the human primatebrain(PetridesandPandya,2002).BA45andBA47 (in humans),thelattercorrespondingtoBA12inthemonkeybrain, showclearhomologuesintheprimatebrain(seeFig.3).BA44is clearlyidentiﬁableinthehumanbrainandisthoughttobeacen- tralbrainregionforhumanspeechprocessing(Friederici,2012).

Petrideset al. (2005) recentlydescribed a cytoarchitectonically similarareainmacaquemonkeys.ThesubregionsintheIFCseem tohave equal representationin both theleftand therightIFC.

Althoughearlystudiesseemtodemonstratealeftwardadvantage, especially for some componentsof language-related Brodmann areas(BA44/45),areviewofallavailabledatadoesnotsupport anystronglateralization(Kelleretal.,2009).

Connectivityanalyseshaveshownstrongconnectionsbetween the IFCand lateraltemporal cortex areas.The fronto-temporal connectionshavebeendescribedindetailforthelefthemisphere astheunderlyingbrainnetworkforspeechprocessing.Connection

Fig.3. MapsoftheIFC(A)inthehumanand(B)inthemacaquebrain.HighlightedarethecytoarchitectonicsubdivisionsofIFCinBA47/12,BA45,andBA44asthemost dominantlanguage-sensitivebrainregionsandtheregionssensitivetoconspeciﬁcvocalizations(basedon:PetridesandPandya,2002).Abbreviations:asarcuatesulcus,cs centralsulcus,ifsinferiorfrontalsulcus,lslateralsulcus,psprincipalsulcus.(Forinterpretationofthereferencestocolorinthisﬁgurelegend,thereaderisreferredtothe webversionofthearticle.)

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studies in macaque monkeys have shown connectivity of BA 47/12to theanterior inferiortemporal cortex and of BA45 to theposteriortemporalcortex(PetridesandPandya,2002).These connectionsmightbetheprecursorsofthehumanventral(from anteriorSTG toBA45 and toBA47/12/fOP) and dorsalspeech processing streams (from posterior STG to B44/6) (Friederici, 2012), which gradually develop in the primate lineage (Rilling etal.,2008).Asimilarfronto-temporalnetworkisthoughttoexist intherighthemisphere,buttheavailabledataaresparse.Theright posteriorSTGseemstobeconnectedtotheanterior(Ethoferetal., 2012)andposteriorregionsoftherightIFC(GlasserandRilling, 2008), buttheseconnectionsarenot reliablyidentiﬁableacross participants(GlasserandRilling,2008).

3. AgeneralfunctionalroleoftheIFC

Although the IFC is strongly associated with speech and prosodyprocessing,itsfunctionsseemnottobelimitedtospeech processing.GiventhegeneralviewthattheIFCislinkedtoseveral first-orderexecutiveprocesses,suchasstimuluscomparisonsor thejudgmentofstimuli(Petrides,2005),itmightspecificallyserve severalself-referencedorother-referencedsocialprocesses,such astheevaluation(Marumoetal.,2009),categorization(Frühholz etal., 2009,2012), and memoryencoding of emotional stimuli (Sergerieetal.,2005).TheIFCmightalsobeinvolvedincontrol- ling,overriding,orinhibitingbehavioralandemotionalresponses (Aronetal.,2004;DillonandPizzagalli,2007;Mitchell,2011),as wellasmirroring(Leslieetal.,2004),empathizing(Schulte-Ruther etal.,2007),orimitatingthebehaviorofotherindividuals(Leeetal., 2006).Allofthesesociallyrelevantprocessescanberegardedas first-orderexecutiveprocesses.

ActivityintheleftbutalsointherightIFCisthusfoundfor differenttasks,especiallyfornonlanguagetasks,whichallinvolve cognitiveprocessingofﬁrst-orderexecutiveprocessesforexter- nalorinternalverbalandnonverbalsocialinformation,especially meaningfulsocialoremotionalinformation.Acommonperspec- tiveforbothverbalandnonverbalprocessingintheIFCmightbe thegeneralproposalthattheIFCintegrates(Hagoort,2005)and performsﬁrst-order executiveprocesses (Petrides,2005).These processesareperformedoninformation,whichisrepresentedin posteriorassociationcorticesaftersensoryprocessingin lower- levelsensoryregions,particularlyintheauditorycortex(Frühholz andGrandjean, 2012).For thecaseof auditoryverbaland non- verbalinformation,thissuggeststhattheIFCperformsexecutive processesonauditoryvoiceinformationprovidedbyhigher-level auditoryregionsintheSTG.

FortheSTG,ithasbeenrecentlysuggestedthattheanteriorSTG (aSTG)andtheposteriorSTG(pSTG)representandprovidediffer- enttypesofauditoryinformationaspartofadualstreammodel forauditoryprocessing.Aventralstreamoriginatinginprimary and secondary auditoryregions, passing through theaSTG and terminatingintherostro-ventralIFC,isthoughttoprovideinvari- antsoundrepresentationsforperceptualconstancy.Forexample, globalacousticcharacteristicsofemotionalvocalizationsprovide perceptualconstancyevenwhentheiractualacousticperformance differs(e.g.emotionalvocalizationsexpressedbyamaleorafemale voice).ThedorsalstreampassingthroughthepSTGandtheinfe- riorparietallobule(IPL)andterminatinginthecaudo-dorsalIFC insteadprovides auditory sequence information for temporally extendedsounds(Rauschecker,2012).Thelattermightrepresent differentdynamic features ofvocalexpressionsat thetemporal frequencyof speechsegmentsand ona suprasegmentalspeech level.Thisdualstreammodelhasbeendescribedonlyfortheleft hemisphere,butcomparable structuralhard wiringintheright hemisphere(Catanietal.,2012;ThiebautdeSchottenetal.,2012)

might suggest similar dual streampathways there, thoughthe evidenceforthelatterislessconsistent(Catanietal.,2007;Rilling etal.,2008).Togetherwiththenotionthatleftandrightauditory regionsparse thespeechsignalatdifferenttime scales(Giraud etal.,2007;Poeppel,2003),theseobservationsmightsuggestthat theleftandrightIFChaveaccesstotemporalacousticinformation ofvocalintonations,whicharedifferentlysampledintime.Atem- poralresolutionoftheleftSTGofabout20–50msprovideshigh temporalresolution,whiletherightauditorycortexsamplesthe sensorysignalin100–300mstimebins,allowinglesstemporalbut improvedspectralandpitchresolution(ZatorreandBelin,2001).

SimilartotheleftandrightSTG,theleftandrightIFChavebeen showntobepredominantlysensitivetoslowandtofastdynamics inspeechandnon-speechsounds,respectively(Husainetal.,2006).

Additionally, the rightIFC is more sensitive toenhanced pitch variationsinspeechcomparedwiththesensitivityoftheleftIFC tomoremonotonouspitchintonatedspeech(Merrilletal.,2012).

Intonationssuperimposedonspeech(BanseandScherer,1996;

JuslinandLaukka,2003)andparaverbalspeech(Pateletal.,2011) and in nonverbal expressions of emotions (Sauter et al., 2010) haveglobalvocalfeatures(i.e.meanintensityorpitch;spectral centerofgravity;harmonics-to-noiseratio,HNR),butalsoshow slowandfastdynamicmodulationsoffeatures.Thesemodulations rangefromultrafastdynamicpitchandintensitymodulationsona cycle-by-cyclebasis(i.e.jitterandshimmer)tofastmicrostructural spectral,pitch,andintensityirregularitiestoincreasedpitchand intensityvariabilityonasegmentalandsuprasegmentallevelin speech.Whileglobalfeaturesmightberepresentedandstoredas invariancesintheventralstream,dynamictemporalmodulations mightbedecodedinthedorsalstreambyparsingthespeciﬁctem- poralintonationpatternsinemotionalvocalizations.

Thefunctionalrole oftheIFCmightbeaunificationofthese differenttypesof auditoryvoiceinformationrepresentedinthe STG(Hagoort,2005).TheIFCaccordinglymightperformfirst-order executiveprocessesonauditoryinformationofemotionalvocali- zations.Specifically,foremotionalvoicesithasbeensuggestedthat theIFCissensitivetothelevelofexplicitnessoftheemotionalcues andwouldbemoreinvolvedintheexplicitcognitiveevaluationof theemotionalvalueinvocalizations.Theavailabledatasupportthe notionofacognitivecontrolledevaluation.Butthisseemsnotto berestrictedtoanexplicitattentivefocusontheemotionalcues invoices,giventhatIFCactivitywasalsofoundwhentheemo- tionalvalueofvoiceswasprocessedpreattentively,suchaswhen itwaspresentedoutsidethefocusofattention(Belinetal.,2008a;

Buchananetal.,2000;Fecteauetal.,2005;Frühholzetal.,2012;

Morrisetal.,1999;Sanderetal.,2005;Wildgruberetal.,2004, 2005).

4. OriginsoftheIFCsensitivitytovocalintonations

Thus,thereisabundantevidenceforIFCsensitivitytoemotional vocalizations.Recentstudiessuggestthatthissensitivityhasphy- logeneticandontogeneticprecursors.Nonhumanprimatesalready usevocalizations for transmitting socially meaningful information,which quiteofteninvolvesthesignalingofemotional and motivational states (Romanski and Averbeck, 2009). Studies in macaquemonkeyshaveshownthat vocalizationscanformdis- cretecategoriesbasedontheirspectro-temporalacousticprofile (AverbeckandRomanski,2006).Thesecategoriesmightbegen- eratedfromacousticcuesandrepresentedintheanteriorventral stream(Rauschecker,2012)andcategorizedbytheIFC(Cohenetal., 2006,2009;Giffordetal.,2005;Russetal.,2008b).Indeed,recent animalstudieshaveidentifiedneuronsintheIFC(seeFig.4)thatare sensitivetoconspecificmeaningfulvocalizations(Romanskietal., 2005).Insteadoflow-levelauditoryfeatures,theseneuronsseemto

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Fig.4.ApproximatelocationsofsinglecellrecordingsitesinmacaquestudiesintheleftandrightIFC,usuallyreferredtoastheventro-lateralprefrontalcortex(vlPFC).

SinglecellactivitywasusuallyrecordedinBA45AandBA9/46v,bothlocatedrostrallytoBA8Avbelowtheprincipalsulcus.Color-codeddotsrefertothefollowingstudies:

(Giffordetal.,2005), (AverbeckandRomanski,2006;Romanskietal.,2005), (Cohenetal.,2007,2009;Russetal.,2008a), (RomanskiandGoldman-Rakic,2002), (Cohenetal.,2006), (Leeetal.,2009;Russetal.,2008b), (Sugiharaetal.,2006),and (Gil-da-Costaetal.,2006)foractivityinthevPM.Abbreviations:asarcuate sulcus,cscentralsulcus,ipdinferiorprecentraldimple,lslateralsulcus,psprincipalsulcus,vpmventralpremotorarea.

decodehigher-orderinformationconveyedbythosevocalizations (Cohenetal.,2007,2009).Thisdecodingisprobablybasedona sensitivitytotheacousticmorphologyofconspeciﬁcvocalizations (Romanskietal.,2005),whichhelptodifferentiateseveraltypes ofvocalizations(Cohenetal.,2006,2009;Giffordetal.,2005;Russ etal.,2008b).Animalnonverbalvocalizationsofprimatesmight ﬁgureasprecursorsofhumanlanguage(Hauser,1997),giventheir comparabilityofinternalstructure(ZolothandGreen,1979)and theirfunctionalsimilarityinsocialcommunications(Arnoldand Zuberbuhler,2006),aswellasthedevelopmentaltrajectoriesinthe underlyingcorticalnetwork(Gil-da-Costaetal.,2006;Rauschecker, 2012;Rillingetal.,2008;ThiebautdeSchottenetal.,2012).

Interestingly,thehumanIFCissensitivetoanimalnonverbal vocalizations(Belinetal.,2008a)andtohumannonverbalvocali- zations(Fecteauetal.,2005),whichsharesomesimilaritieswith vocalizationsofnonhumanprimates.Thisprovidesevidencefora linkintheprocessingofprimatevocalizationsacrossspecies.Sim- ilarly,studiesinhumaninfantshaveshownthattheIFCissensitive tononverbalfeaturesofhumanspeech,especiallyforemotional intonations(Chengetal.,2012;Grossmannetal.,2010),suggesting anearlyontogeneticsensitivitytoconspeciﬁcvocalizations.Sensi- tivityofthehumanIFCtononverbalvocalizationsmightbethe ﬁnalprecursortoemotionalintonationssuperimposedonspeech utterances,becausebothsharesimilaritiesofseveralfeaturesof acoustically encoded emotional cues(Banseand Scherer, 1996;

Pateletal.,2011;Sauteretal.,2010)andoftenappearinthesame context.

Bothnonhumanandhumanprimatestudiesseemtoindicate thattheIFCsensitivityimplieslateralizationchangesduringonto- geneticmaturationand development,resultinginanincreasing leftwardlateralization.Nonhumanprimatesshowamajordevel- opmentaltrajectory frombilateralprocessing toa stronger left hemispherebiasinadults(HauserandAndersson,1994)forsen- sitivitytothecommunicativevalenceofvocalizations(Petersen et al., 1984) (but see: Gil-da-Costa and Hauser, 2006). Human infantsshowastrongerinvolvementoftherightIFC(Chengetal., 2012;Grossmannetal.,2010),whichdevelopstoabilateralrep- resentationinadulthumans.Bothdevelopmentaltrajectoriesin monkeysandinhumansthusshowthatthefunctionalroleofthe leftIFC(relativetotherightIFC)becomesmoreimportantdur- ingdevelopment,highlightingthenotionthattheleftIFCplaysan equallyimportantrolefortheprocessingofvocalemotions.How- ever,trainingofrightIFCactivityinadultscanalsostrengthenthe rightIFCnetwork(Rotaetal.,2011),pointingtothepossibilitythat

boththeleftandtherightIFCaresusceptibletotraininginﬂuences anddevelopmentalchanges.

5. ThefunctionalroleoftheIFCinprocessingemotional vocalizations

TheIFCthusseemstobesensitivetoemotionalvocalizations, and this sensitivityseemstohave developmentalprecursorsin nonhumanprimatesandininfants.TheIFCisprimarilyassumed toexplicitlyandcognitivelyevaluatetheemotionalvalueofvoices (Ethoferetal.,2012;Leitmanetal.,2010),suchasoccursinthe evaluation, labeling,or categorizationofvocalexpressions. This conclusionarisesfromthefactthatstudiesusuallyfindIFCactivity whenparticipantsareaskedtoattentivelyandexplicitlyfocuson theemotionalvalueofvoices(Beaucousinetal.,2007;Ethoferetal., 2006;Mitchell,2006;Wildgruberetal.,2002),orwhenthedecod- ingbecomesmorechallengingbecauseofambiguousacousticcues (Leitmanetal.,2010;Schirmeretal.,2004)orconflictingemotional cues(Leitmanetal.,2010;Schirmeretal.,2004).Bothconditions, theattentiveandexplicittask,aswelltheconditionsofmorechal- lengingdecoding,representfirst-orderexecutiveprocesses.These activeprocessesmightdependonspecificconnectionsofIFCsub- regionswithdifferentsubregionsinthesuperiortemporalcortex, asdefinedbythedifferentauditorypathwaysoutlinedearlier.

Compellingevidencefrompatientstudies(RossandMonnot, 2011), neuroimaging studies (Mitchell et al., 2003), and infant studies(Chengetal.,2012;Grossmannetal.,2010)supportsthe viewthattherightIFCinparticularispredominantforthiscog- nitivelycontrolledevaluationofemotionaltonesofvoices.Recent neuroimagingstudiesfoundseveralrightIFCpeakactivationsdis- tributedfromtheposteriortotheanteriorIFClocatedinBA44 (Frühholzetal.,2012;Kotzetal.,2003),BA45(Bachetal.,2008;

Beaucousinetal.,2007;Ethoferetal.,2006;Sanderetal.,2005), andBA47(Bachetal.,2008;Beaucousinetal.,2007;Belinetal., 2008a;Ethoferetal.,2009;Frühholzetal.,2012;Mitchell,2006;

Sanderetal.,2005),aswellasinthefOP(Frühholzetal.,2012;Kotz etal.,2003;Mitchelletal.,2003;Schirmeretal.,2004)(seeFig.2).

Recently,ithasbeenshownthattheabilitytocontrolactivityinthe rightIFC(BA45)canimproveemotionalprosodyrecognition(Rota etal.,2011).RightIFCactivityisalsoinvolvedduringcognitively more demandingemotionaldecoding in thecase ofambiguous acousticcuesinvoices(Leitmanetal.,2010).Conversely,disrup- tingactivityintherightposteriorIFC(fronto-parietaloperculum)

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(Hoekertetal.,2008)andmid-rightIFC(BA45/46)(Hoekertetal., 2010)canimpairtherecognitionofemotionalprosody.

Interestingly,thelatterstudyalready providesevidencethat disrupting the left IFC (BA 45/46) can also impair emotional prosody recognition,especially for fearfulexpressions (Hoekert etal., 2010).Thissuggests thatnot onlytheright IFC,but also the left IFC, might have a generic role during the processing of emotional voices. Left hemispheric and particularly left IFC lesionsresultinimpairmentsduringtheprocessingofemotional vocalizations(Pell,1998), though righthemisphere lesions still showa morepervasiveinsensitivitytoemotionalprosody(Pell, 2006).However,ithasbeensuggestedthattheleftcomparedwith therightIFChasonly asupplementaryprocessingrole,suchas prosody-relatedworkingmemoryprocesses(Ethoferetal.,2009;

Wildgruberet al., 2005), linguisticprocessing (Buchanan et al., 2000;Wildgruberetal.,2004),retrievalofsemanticknowledge (Beaucousinetal.,2007),orsemanticprocessingduringimpaired prosody processing (Mitchell, 2006; Schirmer and Kotz, 2006;

Schirmeretal.,2004).Nonetheless,evenwhencontrollingforall secondaryandlanguage-relatedtaskeffects,emotionalvocaliza- tionsstillelicitactivityintheleftIFC(Frühholzetal.,2012;Kotz etal.,2003;Leitmanetal.,2010;Sanderetal.,2005).Furthermore, theleftIFCisactiveinresponsetononverbalexpressionswithout anylanguage-relatedfeatures(Belinetal.,2008a;Fecteauetal., 2005; Morris et al., 1999). Both facts argue against a simple supplementaryorspeech-relatedroleoftheleftIFC.

TheseresultstogethersuggestthatboththeleftandtherightIFC areinvolvedintheprocessingofemotionalvaluefromvoiceswith noclearlateralityeffects(Kotzetal.,2003).Summarizingthepeak activationsacrossallfMRIandPETstudiesonprocessingemotional vocalizationsprovidesaclearpictureforabilateraldistributionof peakactivation(seeFig.2).Insteadofaleft-rightdistinction,itturns outthatthenatureorthemediumofvocalexpressions(emotional prosodyversusnonverbalexpressions),aswellasthetasksper- formedonvoices,whichmanipulatedtheattentionalfocusduring theprocessingofvocalexpressions,caninﬂuencethedistribution ofthesepeakactivationsacrossdifferentsubregionsoftheIFG.

6. LeftandrightIFCsubregionsforthedecodingof emotionalvocalizations

6.1. Attentionalfocus:attentiveandpreattentiveprocessingof emotionalvocalizations

Studiesontheprocessingofemotionalvocalizationsusuallyuse differenttasksbymanipulatingtheattentionalfocus(seeFig.1).

Studiesaskparticipantseithertoexplicitlyfocusontheemotional valueofavoice,which allowscognitiveevaluation oftheemo- tionaltoneofavoice(explicitattentionalfocusortask),ortofocus onanothernonemotionalfeatureofthevocalutterance(implicit attentionalfocusortask).Forthelattertask,itisassumedthatthe emotionaltoneofavoiceisstillprocessedonanimplicitorpreat- tentivelevel,givenitsimportanceforadaptivebehavior.Although theIFCis generallysupposed todecodetheemotional valueof voiceswhenparticipantsareaskedtoexplicitlydecodeandlabelits emotionalvalence,recentstudiesalsoconsistentlyfoundIFCactiv- itywhentheemotionaltoneofavoicewaspresentedoutsidethe focusofattention(Belinetal.,2008a;Fecteauetal.,2005;Morris etal.,1999;Sanderetal.,2005;Wildgruberetal.,2004,2005).Early studiesonemotionalvoiceprocessingsuggestedthatanexplicit focusisassociatedwithleftIFCactivity,whereasanimplicitfocus elicitsrightIFCactivity(Buchananetal.,2000).Thisleft(Bachetal., 2008)orrightlateralization(Wildgruberetal.,2005)isalsosup- portedbyotherstudies(Sanderetal.,2005).However,somestudies donotsupportclearlateralization,butratherprovideevidencefor bilateralIFCinvolvementforbothexplicit(Beaucousinetal.,2007;

Ethoferetal.,2006,2009;Schirmeretal.,2004;Wildgruberetal., 2002)andimplicittasks(Belinetal.,2008a;Frühholzetal.,2012;

Morriset al.,1999), allowingnospeciﬁc lateralizedassignment accordingtotheattentionalfocus.

Explicit and implicit tasks during vocal emotion processing seem, however, to elicit activityin different subregions of the IFC.Whereasexplicittasksareabletoelicitactivityinallsubre- gionsofthebilateralIFC,implicit tasksseem toinduceactivity onlyinrostro-ventralIFCareas.Theserostro-ventralareasarethe mainterminationareasoftheventralauditorypathwayprovid- ingaccesstoinvariantobjectorfeatureinformationintheaSTG, whereasthedorsalstreamprovidestemporalpatterninformation (Rauschecker,2012).Thismightsuggestthattheexplicitprocessing ofemotional vocalizationsreliesboth onthetemporalpatterns in emotional voicesand on generaland global object informa- tionofacousticpatterns.Thedecodingofthetemporalpatternis especiallynecessaryforprocessingemotionalprosody,andonly prosodiccuesextendingoverseveralspeechunitsallowvalidcate- gorizationsofemotionalprosodiccues(PellandKotz,2011).Unlike explicitprocessing, which allows one totemporally follow the dynamicchangesinthetemporalpatterns,implicitprocessingof emotionalvocalizations mightrely onlyonthesound-invariant impressionofacousticpatternsinemotionalvoices.

6.2. Themediumofvocalexpressions

Attentionalfocus duringtheprocessing of emotionalvocali- zationsﬁguresasatop-downfactor,whichadjuststhecognitive andthebrainsystemstoprioritizecertainfeaturesofthestimulus.

Thistop-downfactorcaninﬂuencethedistributionofpeakactivity intheIFCinresponsetoemotionalvocalizations,asdiscussedin theprevioussection.However,itseemsthatthemediumofvocal expressionsasabottom-upfactorcanalsoinﬂuencethispeakdis- tribution.Concerningthismediumornatureofvocalizations,vocal expressionsofemotionscanbepurelynonverbal,suchaslaughs, cries,orscreams(Sauteretal.,2010;Simon-Thomasetal.,2009), buttheycanalsobesuperimposedonsemanticallyneutral(Ethofer etal.,2009;Kotzetal.,2003;Leitmanetal.,2010)andsemanti- callyemotionallanguage(Beaucousinetal.,2007;Mitchell,2006;

Mitchelletal.,2003;Schirmeretal.,2004),aswellasonpseu- dospeech(Bach etal.,2008;Frühholzetal.,2012;Sanderetal., 2005).Giventhisdistinctionbetweennonverbalvocalexpressions andemotionalprosody,itmightbeassumedthatemotionalintona- tionssuperimposedonspeechstronglyengagetheleftIFC,whereas nonverbalexpressionsactivatetherightIFC(Meyeretal.,2005).

However,foremotionalprosodyandnonverbalvocalexpres- sions,thereisnoconvincinglateralityeffectforthedistributionof peakactivationsacrossstudies.Similartothecaseforattentional focus,peakactivationsaccordingtothemediumofvocalexpres- sionseemtogroupalongarostro-ventraltocaudo-dorsalaxisin thebilateralIFC.Whereasemotionalprosodyelicitsactivityacross allsubregionsoftheIFC,nonverbalexpressionselicitactivityonly inmoreanteriorregionsoftheIFC.Nonverbalexpressionsdonot revealanyactivityinBA44,butthereismoreactivityinanterior IFCregionsextendingintoventralregionsoftheOFC(BA11)and thefOP.Wecouldassumethat,similartoattention-relatedeffects, discriminationforthepurposeofcategorizingandlabelingofnon- verbalexpressions mainlyreliesonglobalinvariantinformation representedintheaSTG,whereasthediscriminationandcatego- rization ofemotional prosody requiresaccess both totemporal patternsandtoacousticinvariantfeatures.Arolefortheposterior IFCinprocessingtemporalpatternsfromemotionalprosodyisalso evidentin impairmentsintheprocessing ofemotional prosody andthetemporalprosodycontourinpatientswithlesionsinthe posteriorIFC(Adolphsetal.,2002;Rohreretal.,2012).Further- more,recentstudiespointtoapossibleroleoftheposteriorIFC

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Fig.5.IFCsubregionsarethoughttohavesimilarfunctionalrolesinboththeleftandtherighthemispherefortheprocessingofemotionalvocalintonations.Wepropose adistinctionfortheprocessingofemotionalvocalizationsintherostro-ventralandcaudo-dorsalIFCinbothhemispheresdependingontheirstructuralandfunctional connectivitytotheSTGinandacrossthehemispheres.Inthelefthemisphere,majorpathwayshavebeenidentiﬁedfortheprocessingofauditoryobjects,especiallyfor speechfeatures,alongaventral(green)anddorsalpathway(red).ThedorsalpathwaysprimarilyterminateintheposteriorIFC(BA6,44,45),whereastheventralpathways terminateintheantero-inferiorIFC(BA47/12,fOP).Thesepathwaysarethoughttofeedtemporalauditorypatternsandauditorysignalinvariances,respectively(so-called

“chunks”;Rauschecker,2012;RauscheckerandScott,2009),forwardtotheIFC.Thepathwayshavebeendescribedindetailforthelefthemisphere,butnotfortheright hemisphere.Althoughthestructuralconnectivityintheleftandintherighthemisphereisthoughttobecomparable(Catanietal.,2012),thecombineddescriptionofthe structuralandfunctionalconnectivityisnonethelesssparse.Studiestodatehaveonlydescribedarightdorsalpathwayforprosodyprocessing(blue)(Ethoferetal.,2012;

Rillingetal.,2008),withnoevidenceforarightventralstream(green,dotted).(Forinterpretationofthereferencestocolorinthisﬁgurelegend,thereaderisreferredtothe webversionofthearticle.)

(PichonandKell,2013)andthecaudallyadjacentpremotorcortex (Warrenetal.,2006)inthepreparationandexecutionof(vocal) motoroutputsinresponsetoperceivedemotionalprosody.Unlike nonverbalexpressions,emotional prosodymore oftenoccursin conversationalsettings,andthusacloseanatomicallinkbetween theposteriorIFCandtheventralpremotorcortexmightsupport perception-actioncyclesinemotionalconversations.

7. Conclusionsandfuturedirections

Weproposeabilateralrostro-ventraltocaudo-dorsalgradient, similartotheleftIFCunificationgradientproposedbyHagoort (2005)forprocessingauditoryspeech.Thegradientthatwepro- posereflectsa distinction inboth theleftand therightIFCfor theprocessing of emotionalvocalizations (see Fig.5).Thisdis- tinctionfollowstheconnectivitypatternsoftheIFC,withauditory processingareasintheSTG,providingaccesstodifferentauditory informationdependingonthestimulusmodalityasabottom-up featureofemotional vocalizationsanddepending ontheatten- tional focus as a top-down factor. Although this definition of IFC-STGconnectivitypatternshasbeendescribedwithmuchdetail inthelefthemisphere,especiallyfortheprocessingofspeechand vocalutterancesingeneral,adetaileddescriptionoftherighthemi- sphereconnectivity pattern based onfunctional data is largely missing(Ethoferetal.,2012;GlasserandRilling,2008).However, afewconclusionscanbedrawnfromthefunctionaldistribution inpeakactivationsintherightIFC,whichcloselyresemblesthe peakdistributionintheleftIFC.Thissuggestsasimilardualstream pathwaymodelintherighthemispheretothatinthelefthemi- sphere.

Inconclusion,theprocessingofemotionalvocalizationsseems nottoberestrictedtotherightIFC,astheleftIFCshowssimilar activityin responsetoemotional vocalizationsastheright IFC.

Furthermore,unlikethesuggestionoflateralityeffectsforatten- tionaltaskdemands(explicitversusimplicit)andforthemedium ofemotionalvocalizations(emotionalprosody versusnonverbal expressions),bothfactorsdeterminethesameintra-hemispheric peakdistribution.Finally,theIFCisnotonlyactiveduringattentive

decodingofemotionalvocalizations,butmoregenerallyservesas acognitiveevaluationunitwhenthedecodingofemotionalcues fromvoicesbecomesmorechallenging.Thissupportstheviewthat theIFCcomesintoplaywhenﬁrst-orderexecutiveprocesses(as deﬁnedinSection3)areneededforthejudgmentandevaluation ofsociallymeaningfulstimuli.

Thus,itseemsthatbroadevidenceisavailableforthefunctional roleoftheIFCinprocessingemotionalvocalizations,butthatopen questionsremain,aswellassomelimitationsinthepresentreview, whichshouldbeaddressedinfuturestudies.Theﬁrstlimitationof thepresentreviewisthesmallernumberofstudiesonthecortical processingofnonverbalexpressionscomparedwiththenumberof studiesonemotionalprosody.Althoughtheavailablestudiesshow somereplicableandconsistentIFCactivityfornonverbalexpres- sions, more imaging studiesoncorticalprocessing arestrongly neededandshouldprovidemoreconsistentevidenceforourpro- posalofafunctionaldistinctionintheIFC.Similarly,morestudies areneededontheexplicitandattentiveprocessingofnonverbal vocalexpressions.Mostofthestudiesontheprocessingofnon- verbalvocalexpressionuseanimplicit(Belinetal.,2008a;Fecteau etal.,2005;Morriset al.,1999)orapassivelisteningapproach (Warrenetal.,2006).Thismakesitdifﬁculttocomparefunctional activationsfortheattentive(explicit)andpreattentiveprocessing (implicit)ofnonverbalemotionalexpressionsandtocompletely discern theeffects of theattentional focus and themedium of vocalizations.Thus,ourconclusionsontheprocessingofnonverbal expressionsintheIFCarepartlypreliminaryandhavetobetaken withsomecaution.Futurestudiesmightprovidemoresupportive andconsistentevidenceforthedecodingofnonverbalexpressions intheIFC.

Asecondopenquestionconcernsthevocalfeaturesensitivityof theIFC.Futurestudiesshouldinvestigatewhichfeaturesdrivethe discriminationandcategorizationabilitiesoftheIFC.Accordingto nonhumanprimatestudies,theIFCisrathersensitivetohigher- order acoustic information (complex object representations) insteadofﬁrst-orderacousticproperties(simplespectro-temporal features)invocalizations(Cohenetal.,2007).However,discrimi- nationandcategorizationofvocalexpressionsdependsonspeciﬁc