Dynamics of auditory working memory - Frontiers

Working memory denotes the ability to retain stimuli in mind that are no longer physically present and to perform mental operations on them. DownloadArticle DownloadPDF ReadCube EPUB XML(NLM) totalviews ViewArticleImpact SHAREON Abstract Introduction AuditoryWorkingMemoryforNon-spatialSoundFeatures AuditoryWorkingMemoryforSpatialSoundFeatures DirectComparisonsofAuditorySpatialVersusNon-spatialWorkingMemory Summary ConflictofInterestStatement Acknowledgment References Peoplealsolookedat MINIREVIEWarticle Front.Psychol.,11May2015Sec.Cognition https://doi.org/10.3389/fpsyg.2015.00613 Dynamicsofauditoryworkingmemory JochenKaiser* InstituteofMedicalPsychology,GoetheUniversity,FrankfurtamMain,Germany Workingmemorydenotestheabilitytoretainstimuliinmindthatarenolongerphysicallypresentandtoperformmentaloperationsonthem.Electro-andmagnetoencephalographyallowinvestigatingtheshort-termmaintenanceofacousticstimuliatahightemporalresolution.Studiesinvestigatingworkingmemoryfornon-spatialandspatialauditoryinformationhavesuggesteddifferentialrolesofregionsalongtheputativeauditoryventralanddorsalstreams,respectively,intheprocessingofthedifferentsoundproperties.Analysesofevent-relatedpotentialshaveshownsustained,memoryload-dependentdeflectionsovertheretentionperiods.Thetopographyofthesewavessuggestedaninvolvementofmodality-specificsensorystorageregions.Spectralanalysishasyieldedinformationaboutthetemporaldynamicsofauditoryworkingmemoryprocessingofindividualstimuli,showingactivationpeaksduringthedelayphasewhosetimingwasrelatedtotaskperformance.Coherenceatdifferentfrequencieswasenhancedbetweenfrontalandsensorycortex.Insummary,auditoryworkingmemoryseemstorelyonthedynamicinterplaybetweenfrontalexecutivesystemsandsensoryrepresentationregions. Introduction Workingmemoryallowsthetemporarystorageofrelevantinformationanditstask-dependentmanipulation.Itisinvolvedinmanyhighercognitivefunctionsandthusconstitutesafundamentalfunctionofourbrain.Whilemostpreviousresearchhasfocusedonvisualworkingmemory(Drewetal.,2006;LuckandVogel,2013),lessisknownabouttheneuralcorrelatesofauditoryworkingmemory(AWM).Thisbriefreviewsummarizessomeofthemainfindingsonauditoryshort-termorworkingmemory(bothtermswillbeusedinterchangeably)studiesinhumans.Thefocuswillbeonthedynamicsofworkingmemory-relatedprocesses;thereforethereviewislimitedtostudiesassessingnon-invasivemeasuresofneuralactivationwithahightemporalresolution,i.e.,electro-ormagnetoencephalography(EEGandMEG).Mostofthisworkhasconsideredevent-relatedpotentials(ERPs),butsomeinvestigationshavelookedatspectralactivityandatoscillatorycouplingbetweencorticalsources. Evidencefrombothtypesofstudiesspeaksagainsttheexistenceofasingleworkingmemorystoreforauditoryinformation.Instead,activationpatternsvarywiththetypeofmemorizedauditoryinformation,suggestingthatworkingmemoryinvolvesthesamesystemsthatunderlieperceptualprocessing.Soundfeature-specificactivationdifferenceswereparticularlyobviousforcomparisonsbetweensoundidentityandlocation,i.e.,stimulusparametersthatareprocessedintopographicallydistinctcorticalregions(RauscheckerandTian,2000). AuditoryWorkingMemoryforNon-spatialSoundFeatures Theshort-termretentionofpitchelicitsaload-dependentfrontalnegativewave.Usingnon-verbal,pure-tonestimulitoavoidphonologicalorsemanticprocessing,memoryloadeffectsweretestedbypresentingeitherone200-mspuretonetobothearsortwodifferentstimulitoeachear(Guimondetal.,2011).Asustainedanteriornegativewave(SAN)duringthe2-sdelayintervalshowedhigheramplitudesfortwothanoneto-be-rememberedstimulus.ControlexperimentsconfirmedtheroleoftheSANforshort-termmemoryprocessingbyexcludingameresensory-drivenresponseorinternalrehearsal.Comparisonwithavisualshort-termmemoryparadigmshowedthattheSANduringretentionwasspecifictotheauditorytask(Lefebvreetal.,2013).Amemoryload-sensitiveSANwasalsoobservedduringtheretentionofsoundsdifferingintimbreinsteadofpitch(Noldenetal.,2013).ThecorticalgeneratorsofthiswavewereassessedwithMEG.DuringAWMfortonesequences,sourcelocalizationrevealedmemoryload-dependentactivationsinbilateralsuperiortemporal,superiorparietalandfrontalcortex(Grimaultetal.,2009).Astudyinvolvingthecomparisonoftonesequencesofdifferentlengthsidentifiedseveralbrainareaswhoseactivationcorrelatedwiththenumberofsuccessfullymemorizeditems(Grimaultetal.,2014).Theseincludedbilateralsuperior/middletemporalcortexandseveralregionsinbilateralfrontalcortex.ThissourcetopographypartlyoverlappedwithfMRIresults(Gaabetal.,2003;Koelschetal.,2009)andsuggestedthattheretentionofsimpleacousticfeaturesinvolvesthesustainedactivationofsensoryrepresentationsinadditiontofrontalexecutiveregions. ThefrontalnegativityisarobustphenomenonthatwasalsoobservedinERPstudiesemployingverbalsoundsthatmayelicitsemanticprocessingbeyondlow-levelacousticstorage.Asustainedfrontalnegativeshiftwaslargerforaurallythanvisuallypresenteddigits(Langetal.,1992).Similarly,amemoryload-dependentfrontalnegativitywaslargerforspokenthanwrittensyllables(Ruchkinetal.,1997),whereasvisualstimuligaverisetoaposteriorpositivity.TheroleoftheprefrontalcortexforAWMwasfurthersupportedbyastudyinpatientswithfrontalcortexlesions.TheyshowedreducedactivationsbothinauditoryareasandprefrontalcortexandfailedtoattenuatetheirresponsestodistractingtonesduringthedelayperiodofanAWMtask(ChaoandKnight,1998). WhileERPinvestigationsfocusontime-lockedbroad-bandactivity,spectralanalysisistypicallyperformedonsingle-trialbasis,maintainingactivitythatisnotphase-lockedtoadefinedevent.AnalysesofspectralactivityindifferentfrequencybandsmayinformaboutaspectsofprocessingnotcapturedbyERPs.Forexample,activityinthealphaband(8–12Hz)hasbeenrelatedtoactiveinhibitionofinterferingprocessing(Klimeschetal.,2007;JensenandMazaheri,2010),andgammaactivity(>30Hz)hasbeenlinkedtoobjectrepresentations,attentionandmemory(KaiserandLutzenberger,2003;Jensenetal.,2007).Moreover,coherenceorphasesynchronizationcalculatedonthebasisofspectralsignalsprovideinformationaboutcortico-corticalinteractions. IncreasesofspectralpowerandsynchronizationoverfrontalcortexcharacterizedAWMfordifferenttypesofnon-spatialsounds.DuringthemaintenancephaseofanAWMtaskrequiringthememorizationofsounddurations,wefoundincreasedgammaactivity(70–80Hz)overprefrontalcortex(Kaiseretal.,2007b).Asimilarresultwasobtainedforartificialsyllablesvaryinginvoiceonsettimeandformantstructure.Heregammaactivity(65–70Hz)wasincreasedoverleftanteriortemporal/inferiorfrontalcortex(Kaiseretal.,2003).Gammacoherencebetweentheputativesensoryrepresentationregionsandprefrontalcortexshowedasustainedincreaseacrossthedelayphase(Kaiseretal.,2005),possiblyreflectingenhancedcross-talkbetweenstorageandexecutivenetworksunderlyingstimulusmaintenance.RightfrontalalphaandrighttemporalbetaactivitycorrelatedpositivelywithmemoryloadduringthedelayperiodofaSternberg-typetaskusingnaturalsyllables(Leibergetal.,2006b).Thealphaincreasewasconsistentwithotherauditory(Luoetal.,2005;Kaiseretal.,2007a;Kawasakietal.,2010)andvisualshort-termmemorystudies(Sausengetal.,2005,2009)andmayhavereflectedincreasedexecutivedemandsand/orthesuppressionofirrelevantprocessing. AuditoryWorkingMemoryforSpatialSoundFeatures MEGstudiesinvestigatingspatialAWMtaskswithfilterednoisesoundsfoundgammaactivityoverregionsoftheputativeauditorydorsalspaceprocessingstream(RauscheckerandTian,2000).Whencomparingauditoryspatialworkingmemorywithanon-memorycontraltask,bothmaintenanceandretrievaloflateralizedsoundswereaccompaniedbyincreasedparietalgammaactivity(55–70Hz)(Lutzenbergeretal.,2002;Leibergetal.,2006a).Inaddition,enhancedfrontalgammaactivitywasfoundduringthefinal100msofthemaintenanceperiod.Asinourstudywithartificialsyllablesdescribedabove(Kaiseretal.,2003),gammacoherencebetweentheputativesensoryrepresentationregionsandfrontalcortexwasincreasedduringthedelayphase. Inspiredbythehypothesizedroleofgammaactivityforsensoryrepresentations(Jensenetal.,2007),wesearchedforspectralsignaturesoftheshort-termmaintenanceofindividualauditorystimulibycontrastingdelay-periodactivationsbetweenindividualmemorystimuli.WeperformedFastFourierTransformsonsingletrialsforabout1.5Hz-widefrequencybinsacrossthegammarange.Theproblemofmultipletestingwasaddressedbyapplyingastatisticalprobabilitymappingbasedonpermutationtests.Whenfrequencyrangesshowingsignificantdifferencesbetweenstimuliwereidentified,thedatawerefilteredinthesefrequenciestoassessspectralactivitytimecourses. Weidentifiedstimulus-specificcomponentsofgammaactivityduringthemaintenanceofdifferentsoundlateralizationangles(Kaiseretal.,2008).Samplestimuliwere200-msnoisesconvolutedwithhead-relatedtransferfunctionstocreatevirtuallateralizationanglesofeither15°or45°withrespecttothemidsagittalplane.Afteran800-msdelayperiod,thesestimulihadtobecomparedwithteststimulithatcouldeitherbepresentedwiththesame,withamoremedialoramorelateralangle.Participantswereassignedtotwogroupswhowerepresentedwithonlyright-orleft-lateralizedstimuli,respectively.Forbothgroups,stimulus-specificgammaactivity(55–70Hz)wasfoundoveroccipito-parietalcortexcontralateraltostimulation.Thistopographycouldbeconsideredconsistentwiththeauditorydorsal“where”stream,butmightalsoindicateaninvolvementofvisualspatialimagery.Gammaactivitywasmostpronouncedatlatenciesof200–500msaftersoundoffset,i.e.,inthemiddleofthe800-msdelayphase. Thistimingofstimulus-specificgammaactivitycouldeitherhavereflecteddelayedresponsestomemorysoundsorpreparatoryactivationsprecedingtheteststimuli.Todecidebetweenthesepossibilities,afollow-upstudyuseddelaydurationsofeither800or1200msinseparaterecordingblocks(Kaiseretal.,2009b).ThemainresultsofthisstudyaredepictedinFigure1.Wereplicatedstimulus-specificgammaactivity(75–100Hz)overcontralateralposteriorcortex.Fortheshorterdelayduration,thisactivitypeakedagaininthemiddleofthemaintenancephase,i.e.,about400msaftertheoffsetofthememorystimulus.Incontrast,stimulus-specificactivitywasclearlydelayedforthelongerdelayduration,peakingataround800msaftermemorystimulusoffset.Inotherwords,gammaactivityreacheditsmaximum400msbeforetheonsetoftheteststimulusforbothdelaydurations.Thetimecourseofstimulus-specificactivitythusseemedtoreflecttheactivationoftask-relevantinformationinpreparationforcomparisonwiththetestsound. FIGURE1 Figure1.Stimulus-specificgammaactivitytosoundsofdifferentlateralizationangleinaspatialAWMtask.Thegraphontheleftshowsgrand-averagetimecoursesofagammaactivitydifferentiationscorereflectingthedegreetowhichoscillatorysignalsdifferentiatebetweenthetwosamplestimuli.Positivevaluesindicatea“consistent”differentiationwithlargeramplitudestothepreferredstimulus,whilenegativevaluesstandforan“inconsistent”differentiationwithlargeramplitudestothenon-preferredsound.Theamplitudeofthisdifferencescorewastestedagainstzerotoobtainastatistical(p-value)timecourse.CurveswereoverlaidforbothdelaydurationsandalignedforthetimepointofS2.Theredcurve(referringtothetimeaxisatthetop)showstheshort,thegreencurve(referringtothetimeaxisatthebottom)thelongdelayperiod.Themapontherightshowsthesensorpositionsshowingstimulus-specificeffectsforthelateral(l)andmedial(m)samplesoundsduringtheshort(redcircles)andthelong(greencircles)delaydurations.AdaptedfromKaiseretal.(2009b),copyright2009withpermissionfromElsevier. Wealsoexaminedtherelationshipbetweenstimulus-specificgammaactivityandtaskperformance.Ifthesesignalsreflecttheactivationoftask-relevantinformation,theyshouldpredicttheaccuracyofthecomparisonwiththeteststimuli.Inbothstudies(Kaiseretal.,2008,2009b),wefoundpositivecorrelationsbetweentaskperformanceandgammaactivityduringthefinalpartofthedelayphase.Exploringthenatureofthisrelationshipfurther,wecomparedgammaactivitytimecoursesbetweenbetterandpoorerperformers.Interestingly,neithergroupdifferedintheabsolutemagnitudeofstimulus-specificactivationsbutintheirtiming.AsshowninFigure2,betterperformersshowedamoresustainedrepresentationofthememorizedinformationuntiltheendofthedelayperiod.Correlationsbetweengammaactivityandperformancehavebeenreportedinawidevarietyofparadigms(Riederetal.,2011).Heretheysupportedthefunctionalrelevanceofactivatingrepresentationsofthesamplesoundsforaccuratecomparisonswiththeteststimuli. FIGURE2 Figure2.Timecoursesofthedifferentiationscore(seelegendtoFigure1)forgoodandbadperformers(inblueandred,respectively)fortheshortdelayduration(A)andthelongduration(B)inthestudybyKaiseretal.(2009b). DirectComparisonsofAuditorySpatialVersusNon-spatialWorkingMemory Studiesthatcomparedworkingmemoryforsoundlocationsandsoundpatternsdirectlysupportedthenotionofdorsalandventralstreamsfortheprocessingofauditoryspatialandnon-spatialinformation,respectively(RauscheckerandTian,2000).Inlinewiththisdual-streammodel,positiveERPdeflectionsat300–500msafterbothmemoryandteststimuliwerefoundatfronto-temporalelectrodesforanon-spatialAWMtaskandatcentro-parietalelectrodesforaspatialtaskwith500-msnoisebursts(Alainetal.,2001).Positivemaintenance-relatedERPshiftsduringthenon-spatialtaskareatoddswiththeSANreportedabove(e.g.,Guimondetal.,2011;Lefebvreetal.,2013).However,severaldifferencesbetweenstudiesmakeithardtocomparethesefindingsdirectly:Alainetal.(2001)usedlongerandspectrallyrichersoundsandamuchshorterdelaydurationthanthestudiesreportinganSAN(500versus2000ms,respectively),raisingthepossibilitythatechoicmemorymayhavebeeninvolvedratherthanshort-termmemory.Moreoverdatawereshownfromafewselected(e.g.,fronto-temporal)electrodesitesonly,whereastheSANwasmostpronouncedatmidlinefronto-centralsites. DifferencesbetweenauditorylocationandpitchworkingmemorywerefoundalsofortheN1componenttopuretonesservingasteststimuli,suggestinganearlyonsetofsegregatedprocessingatabout100ms(Anourovaetal.,2001).TheN1findingswerereplicatedinasubsequentstudyrequiringthememorizationofeitherlocationorfrequencyofshortsoundsequences(Anurovaetal.,2003).Inaddition,samplesoundselicitedmorenegativeERPsat200and400msinthefrequencythanlocationtaskandmorepositiveERPsat450–650msforthelocationthanfrequencytask.Sourceanalysisoflatepositivepotentialstoprobestimulirevealedapredominantinvolvementofmiddletemporalcortexinpitchandofoccipito-temporalregionsinlocationprocessing(Anurovaetal.,2005).Incontrast,alateslowwavewasmodulatedbymemoryloadbutdidnotdifferbetweentasks. Inlinewiththestudiesreportedabovethatusedsimplesounds,ann-backworkingmemorytaskwithenvironmentalsoundspresentedatdifferentvirtuallocationsrevealedsegregationbetweenspatialandnon-spatialprocessingfromabout200msonwardsinauditoryassociationcortexandfronto-parietalcortex(Alainetal.,2009).Insummary,theseERPstudiesshowedanearlytopographicalsegregationduringencodingandretrievalofspatialversusnon-spatialauditoryinformationinaccordancewiththedual-streammodel. Followingupourstudiesonstimulus-specificgammaactivitybycomparingnon-spatialandspatialAWMdirectly,wedemonstratedthetask-dependenceofstimulus-specificactivations(Kaiseretal.,2009a).Thesamefilterednoisesoundsthatcoulddifferinfrequencyandperceivedlateralizationwereusedinbothtasks.Separatecomponentsofgammaactivity(50–90Hz)duringthedelayphasedistinguishedbetweenbothstimulusfeatures.Differentlateralizationangleswererepresentedbyposteriorgammaactivity,anddifferentsoundfrequencies,byfronto-centralcomponents.Thesefeature-specificactivationspeakedat200–300msbeforetheonsetoftheteststimulusandshowedacleartask-dependence:amplitudemodulationswereobservedonlywhentherepresentedfeaturewastask-relevant.Taskperformancewascorrelatedbothwithenhancedactivityforthetask-relevantstimulusattributeandreducedactivityforthetask-irrelevantfeature.Thisstudyshowedthatrepresentationsofauditoryfeaturesarereactivateddependingontaskdemandsandthatperformancebenefitsfromactivatingtask-relevantandattenuatingtask-irrelevantrepresentations. Summary Thepresentfindingsareconsistentwiththenotionofworkingmemoryasanemergentpropertyrelyingonthedynamicinterplaybetweenattentionalandsensorysystems(PasternakandGreenlee,2005).EEGandMEGprovidemeasuresofneuralactivitywithasufficientlyhightemporalresolutiontodistinguishencoding,maintenanceandretrievalinAWM.Whilethereissomeevidencefortask-specificdifferencesinERPresponsesduringencoding(Anurovaetal.,2003;LehnertandZimmer,2006),mostofthestudieshavefocusedontheshort-termretentionofacousticinformation.StimulusmaintenanceisreflectedbysustainedERPdeflectionswhosetopographyvarieswiththetask-relevantstimulusfeature.Themaintenanceofnon-spatialsoundattributeslikepitchisaccompaniedbyafronto-centralnegativity(Guimondetal.,2011).Thisslowwavereflectsvariationsinmemoryloadandistopographicallydistinctfrommoreposterioractivationsduringvisualworkingmemory(Lefebvreetal.,2013).Sourceanalysishasdemonstratedgeneratorsinauditoryandfrontalareas,suggestingthattheshort-termretentionofpitchispartiallyaccomplishedbytheprolongedactivationorthereactivationofthebrainregionsunderlyingtheperceptualprocessingofpitch(Grimaultetal.,2014).Incontrast,soundlocationseemstobeprocessedbymoreposterior,parieto-occipito-temporalregions.ThetopographicaldifferencesbetweensoundfrequencyversuslocationprocessinginAWMareconsistentwiththemodelofsegregatedauditoryventralanddorsalstreams,respectively(Alainetal.,2001;KaiserandLutzenberger,2003).ERPworkcomparingindividualsoundfeatureshasdemonstrateddifferentialprocessingofspatialversusnon-spatialsoundparametersstartingfrom100msafterstimulusonset.Thesedifferencespertainedmainlytoencoding,earlymaintenanceandretrievalbutwerelessevidentduringthelaterpartofalongerretentionperiod(Anurovaetal.,2003).Analysesofspectralsignalshavedemonstratedsoundfeature-specificincreasesofgammaactivitybothduringmaintenanceandretrieval.However,representationsoftask-relevantinformationwerenotsustainedacrossthedelayperiodbutweretemporallyrelatedtotheonsetoftheteststimulus(Kaiseretal.,2009b).Incontrast,coherencebetweensensoryrepresentationregionsandprefrontalcortexshowedasustainedincreaseacrossthemaintenancephasesofspatialandnon-spatialAWMparadigms(Lutzenbergeretal.,2002;Kaiseretal.,2003).Insummary,bothencodingandretrievalarecharacterizedbytheenhancedprocessingoftask-relevantstimuliorstimulusattributes.Maintenancereliesonacombinationofaprolongedactivationorareactivationofsensoryrepresentationsandanactivationoffrontalexecutivenetworkswithincreasedcouplingbetweenbothsetsofregions. Whilethemajorityofstudieshavefocusedonthemaintenanceaspectofworkingmemory,researchonmentaloperationsonstoredsoundsisverylimited.Workingmemoryoperationsincludetheselectionofonestoreditemamongstothers,updatingthefocusofattentionorthecontentofworkingmemorywithnewitems,rehearsalandcopingwithinterference(Bledowskietal.,2010).Shiftsofattentiontoauditoryobjectsheldinworkingmemorywereassociatedwiththeactivationoffronto-parietalattentionsystems,andfurthertemporalandparietalactivationsdistinguishedbetweenspatialandcategory-relatedattentioncues(Backeretal.,2015).Mentaltransformationandupdatingofauditorymemorycontentsinvolvedincreasedfrontalandtemporalthetapowerandenhancedfronto-temporalthetaphasesynchrony(Kawasakietal.,2010,2014). WhilewehavegainedsubstantialknowledgeaboutEEG/MEGsignalssensitivetothenumberofauditoryitemsheldinshort-termmemory,futurestudiesmayfocusontheneuronalsignaturecodingtheprecisionofindividualitems(Kumaretal.,2013;Maetal.,2014).Thisrequirescleverexperimentaldesigns,sophisticatedbehavioralanalysesandfine-grainedanalysesofEEG/MEGsignals.Furthermore,analyzingconnectivitymeasuresinEEG/MEGmayhelptoidentifythemechanismsunderlyingdynamicinteractionsbetweenthefronto-parietal“working”systemthatprioritizes,modifiesandprotectsauditoryitemsfrominterferenceandthestoragesystemthatcodeseachitemrepresentationbyasingularactivitypattern.Theseanalysesmayhelptorevealfurthercommunalitiesanddifferencesbetweenvisualandauditoryworkingmemory. ConflictofInterestStatement Theauthordeclaresthattheresearchwasconductedintheabsenceofanycommercialorfinancialrelationshipsthatcouldbeconstruedasapotentialconflictofinterest. Acknowledgment IamgratefultoChristophBledowskiforhelpfulcomments. 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Editedby:TimothyM.Ellmore,TheCityCollegeofNewYork,USA Reviewedby:JonathanR.Folstein,FloridaStateUniversity,USAChristineLefebvre,CentredeRecherchedeL’institutUniversitairedeGériatriedeMontréal,Canada Copyright©2015Kaiser.Thisisanopen-accessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense(CCBY).Theuse,distributionorreproductioninotherforumsispermitted,providedtheoriginalauthor(s)orlicensorarecreditedandthattheoriginalpublicationinthisjournaliscited,inaccordancewithacceptedacademicpractice.Nouse,distributionorreproductionispermittedwhichdoesnotcomplywiththeseterms. *Correspondence:JochenKaiser,InstituteofMedicalPsychology,GoetheUniversity,Heinrich-Hoffmann-Strasse10,60528FrankfurtamMain,Germany,[email protected] ThisarticleispartoftheResearchTopic TheTemporalDynamicsofCognitiveProcessing Viewall 15Articles Peoplealsolookedat Download