Top-down influences on visual processing - Nature

Cortical neurons are subject to top-down influences of attention, expectation and perceptual tasks. 'Top-down' refers to cognitive influences ... Skiptomaincontent Thankyouforvisitingnature.com.YouareusingabrowserversionwithlimitedsupportforCSS.Toobtain thebestexperience,werecommendyouuseamoreuptodatebrowser(orturnoffcompatibilitymodein InternetExplorer).Inthemeantime,toensurecontinuedsupport,wearedisplayingthesitewithoutstyles andJavaScript. Advertisement nature naturereviewsneuroscience reviewarticles article Subjects Sensorysystems KeyPoints Incontrasttothetraditionalideathattheprocessingofvisualinformationconsistsofasequenceoffeedforwardoperations,withneuronalfunctionalpropertiestakingonincreasingcomplexityastheinformationprogressesthroughahierarchyofcorticalareas,increasingevidencepointstowardsareverseprocess,withhigher-ordercognitiveinfluencesinteractingwithinformationcomingfromtheretina. Thus,ratherthanhavingafixedfunctionalrole,neuronsshouldbethoughtofasadaptiveprocessors,changingtheirfunctionaccordingtothebehaviouralcontext. Visionisanactiveprocessinwhichhigher-ordercognitiveinfluencesaffecttheoperationsperformedbycorticalneurons. Visualpathwaysoperatebidirectionally,witheachfeedforwardconnectionbeingmatchedbyfeedbackorre-entrantconnectionsgoingfromhigher-tolower-ordercorticalareas. Top-downinfluencesincludevariousformsofattention,suchasspatial,objectorientedandfeatureorientedattention. Top-downinfluencesarenotlimitedtoattentionbutmediateamuchbroaderrangeoffunctionalroles,includingperceptualtask,objectexpectation,scenesegmentation,efferencecopy,workingmemoryandtheencodingandrecalloflearnedinformation. Theeffectoftop-downinfluencesistochangetheinformationconveyedbyneurons,bothbyalteringthetuningoftheirresponsestostimulusattributesandbychangingthestructureofcorrelationsoverneuronalensembles. Allareasofthevisualpathway,exceptfortheretina,aresubjecttotop-downinfluences,includingearlycorticalstagesofvisualprocessingsuchastheprimaryvisualcortexandthelateralgeniculatenucleus,andallareasalongthedorsalandventralvisualcorticalpathways.Eachareacontainsanassociationfieldofpotentialinteractions,andexpressesasubsetoftheseinteractionstoexecutedifferentfunctions. Thesourcesoftop-downinfluencesarewidespread,witheachareaprovidinginformationreflectingthefunctionalpropertiesofthatarea.Asaconsequence,evenasingleneuroncanbeviewedasamicrocosmofactivityoccurringthroughoutthevisualpathway. Weproposethatthecircuitmechanismoftop-downcontrolandadaptiveprocessinginvolvesagatingofintrinsiccorticalcircuitswithinanareamediatedbylong-rangefeedbackconnectionstothatarea.Byselectingasubsetofinputs,aneuroncanexpressdifferentcomponentsofitsassociationfield,andasaresulttakeondifferentfunctionalroles. AbstractRe-entrantorfeedbackpathwaysbetweencorticalareascarryrichandvariedinformationaboutbehaviouralcontext,includingattention,expectation,perceptualtasks,workingmemoryandmotorcommands.Neuronsreceivingsuchinputseffectivelyfunctionasadaptiveprocessorsthatareabletoassumedifferentfunctionalstatesaccordingtothetaskbeingexecuted.Recentdatasuggestthattheselectionofparticularinputs,representingdifferentcomponentsofanassociationfield,enableneuronstotakeondifferentfunctionalroles.InthisReview,wediscussthevarioustop-downinfluencesexertedonthevisualcorticalpathwaysandhighlightthedynamicnatureofthereceptivefield,whichallowsneuronstocarryinformationthatisrelevanttothecurrentperceptualdemands. Thisisapreviewofsubscriptioncontent,accessviayourinstitution Relevantarticles OpenAccessarticlescitingthisarticle. 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Additionalaccessoptions: Login Learnaboutinstitutionalsubscriptions Figure1:Feedbackpathwayscarryingtop-downinformation.Figure2:Task-dependentchangesinneuraltuningandinformationcontentintheprimaryvisualcortex.Figure3:Neuronsintheprefrontalcortexcarryoutdifferentfunctionsinaccordancewiththetask.Figure4:Learnedassociationgeneratesrecall-relatedactivityinthemedialtemporalarea.Figure5:Task-dependentchangesinlocalfieldpotentialcoherenceandnoisecorrelationsintheprimaryvisualcortex.Figure6:Top-downinfluencesoneffectiveconnectivitywithinandbetweencorticalareas. 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GoogleScholar  DownloadreferencesAcknowledgementsThisworkwassupportedbyUSNationalInstitutesofHealthgrantEY007968(C.D.G.),agrantfromtheJamesS.McDonnellFoundation(C.D.G.),theNationalNaturalScienceFoundationofChinagrant31125014(W.L.)andthe111ProjectB07008(W.L.).AuthorinformationAuthorsandAffiliationsTheRockefellerUniversity,1230YorkAvenue,NewYork,10065,NewYork,USACharlesD.GilbertStateKeyLaboratoryofCognitiveNeuroscienceandLearning,BeijingNormalUniversity,Beijing,100875,ChinaWuLiAuthorsCharlesD.GilbertViewauthorpublicationsYoucanalsosearchforthisauthorin PubMed GoogleScholarWuLiViewauthorpublicationsYoucanalsosearchforthisauthorin PubMed GoogleScholarCorrespondingauthorCorrespondenceto CharlesD.Gilbert.Ethicsdeclarations Competinginterests Theauthorsdeclarenocompetingfinancialinterests. RelatedlinksRelatedlinksFURTHERINFORMATION CharlesD.Gilbert'shomepage GlossaryRe-entrantorfeedbackpathways Processingstrategyinwhichtheproductofanongoingcomputationatonecorticallevelisanalysedbythenextlevel.Theresultantinformationisthensentbacktotheinitialleveltoinfluenceitsfurthercomputation.Thisisalsosometimesreferredtoascountercurrentprocessingstreams. Visualcorticalhierarchy Thehierarchyofcorticalareasintheclassicalmodelofthecorticalrepresentationofvisualinformationbeginningwiththeprimaryvisualcortexandascendingthroughtwopathways:aventralpathwayextendingintothetemporallobe,whichisinvolvedwithobjectrecognition,andadorsalpathwayextendingintotheparietallobe,whichisinvolvedwithvisuallydirectedmovementandspatialattention. Intermediate-levelvision Visualprocessingthatinvolvescontourintegrationandsurfacesegmentation. Distracters Inacomplexvisualscene,someobjectsareattended(thetargets)andothers(thedistracters)areunattended,butthedistracterscancompetewiththetargetforattentionalresources. Hemifield One-halfofthevisualfield. Linelabel Thepropertyorinformationrepresentedbyaneuron.Differentneuronsrepresentdifferentvalues,andthestrengthoftheirfiringindicateshowclosethestimulusistothatvalue. Noise Thevariabilityinneurons'responsestoagivenstimulus.Ifdifferentneuronswithsimilarfunctionalpropertieshaveindependentnoise,anensembleofsuchneuronscancarrymoreinformationaboutastimulusthanasingleneuron. Localfieldpotentials (LFPs).Theelectricalfieldsgeneratedbyapopulationofneurons,withsignalshavingcomponentsspanningaspectrumoffrequencies.LFPsoriginatefromtheintegratedcurrentscomingfromsynapticactivationandfromactionpotentialsindendrites,cellsomataandaxons. RightsandpermissionsReprintsandPermissionsAboutthisarticleCitethisarticleGilbert,C.,Li,W.Top-downinfluencesonvisualprocessing. NatRevNeurosci14,350–363(2013).https://doi.org/10.1038/nrn3476DownloadcitationPublished:18April2013IssueDate:May2013DOI:https://doi.org/10.1038/nrn3476SharethisarticleAnyoneyousharethefollowinglinkwithwillbeabletoreadthiscontent:GetshareablelinkSorry,ashareablelinkisnotcurrentlyavailableforthisarticle.Copytoclipboard ProvidedbytheSpringerNatureSharedItcontent-sharinginitiative Furtherreading Feedforwardandfeedbackinteractionsbetweenvisualcorticalareasusedifferentpopulationactivitypatterns JoãoD.Semedo AnnaI.Jasper ByronM.Yu NatureCommunications(2022) Existingfunctioninprimaryvisualcortexisnotperturbedbynewskillacquisitionofanon-matchedsensorytask BrianB.Jeon ThomasFuchs SandraJ.Kuhlman NatureCommunications(2022) Disentanglingtheflowofsignalsbetweenpopulationsofneurons EvrenGokcen AnnaI.Jasper ByronM.Yu NatureComputationalScience(2022) Hierarchicalandnonhierarchicalfeaturesofthemousevisualcorticalnetwork RinaldoD.D’Souza QuanxinWang AndreasBurkhalter NatureCommunications(2022) Corticalfeedbackloopsbinddistributedrepresentationsofworkingmemory IvanVoitov ThomasD.Mrsic-Flogel Nature(2022) Accessthroughyourinstitution Changeinstitution Buyorsubscribe Advertisement Explorecontent Researcharticles Reviews&Analysis News&Comment Videos Currentissue Collections FollowusonFacebook FollowusonTwitter Subscribe Signupforalerts RSSfeed Aboutthejournal Aims&Scope JournalInformation AbouttheEditors JournalCredits Editorialinputandchecks EditorialValuesStatement JournalMetrics Publishingmodel Editorialpolicies Posters Conferences WebFeeds Contact Publishwithus ForAuthors ForReferees Submitmanuscript Search Searcharticlesbysubject,keywordorauthor Showresultsfrom Alljournals Thisjournal Search Advancedsearch Quicklinks Explorearticlesbysubject Findajob Guidetoauthors Editorialpolicies Closebanner Close SignupfortheNatureBriefingnewsletter—whatmattersinscience,freetoyourinboxdaily. 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