NeurologicaldisordersandthestructureofhumanconsciousnessJeffreyW.Coone - PDF document

NeurologicaldisordersandthestructureofhumanconsciousnessJeffreyW.CooneyandMichaelS.GazzanigaDepartmentofPsychology,DartmouthCollege,6162MooreHall,Hanover,NH03755,USA;currentlyat:HelenWillsNeuroscienceInstitute,UniversityofCalifornia,Berkeley,5201TolmanHall,Berkeley,CA94720,USACenterforCognitiveNeuroscienceandDepartmentofPsychology,DartmouthCollege,6162MooreHall,Hanover,NH03755,USARecentstudiesthatidentifydistinctneuralcorre-latesofperceptualawarenessofferapromising Correspondingauthor:JeffreyW.Cooney(jcooney@uclink.berkeley.edu). TRENDSinCognitiveSciencesVol.7No.4April20031364-6613/03/$-seefrontmatter2003ElsevierScienceLtd.Allrightsreserved.doi:10.1016/S1364-6613(03)00058-5 regionsmightnotonlycorrelatewithspecicperceptualexperiences,butcouldbesufcienttocausethem.IntegratedawarenessemergesfrommodularinteractionswithinaneuronalworkspaceAlthoughevidenceforthemodularityofinformationprocessingisstrong,amodulararchitectureisnot,initself,sufcienttoaccountforthemajorityofcognitivetasksthatoccurwithintherealmofconsciousexperience.Thepresenceofalarge-scalenetwork,whoselong-rangeconnectivityprovidesaneuralworkspacethroughwhichtheoutputsofnumerous,specialized,brainregionscanbeinterconnectedandintegrated,providesapromisingsolutiontothisneedforintegration,andtswellwitharangeofempiricalobservationsoutlinedinthefollowingsections.Althoughthecharacteristicsofsuchanetworkarenotclearcurrently,severalstudiesindicatetheinvolvementofprefrontalcortex,anteriorcingulatecingulateandthalamocorticalinteractionsinteractionsinmechan-ismsthatenablethemobilizationofmodularinformationintoastateoflarge-scalenetworkavailabilityavailability.Intheworkspacemodel,outputsfromanarrayofparallelprocessorscontinuallycompeteforinuencewithinthenetwork[7–9].Dynamicintegrationoftheseoutputs,whichcombinesfactorsincludingbottom-upstimulusattributes,modulationcausedbycontextualvalenceandmemory,andselectiveattentionalamplica-tion,determineswhichaspectsoftheavailableinfor-mationemergeasdominant,andgivesrisetoacoherentnetworkstateinwhichtheintegratedinformationiswidelyavailableandcanbeusedbyavarietyofcognitiveprocessesthatrequireinputfrommultiplemodulesmodules.Theresultofthisprocessisauctuatingstreamoftransientlyself-sustained,self-modifyingworkspacestates,thecharacteristicsofwhicharepostulatedtodeterminethecontentsofthesubjectiveexperienceoftheindividual[9,18].Althoughthemajorityofcerebralproces-singtakesplaceoutsideconsciousawareness,informationisperceivedconsciouslywhenitissufcientlyampliedwithinthesystemtogenerateacoherentnetworkstateinwhichtheinformationiswidelyavailabletoarangeofmodularprocessors.Thepopulationofneuronsactivatedatanygivenmomentthenfurtherinuencesthedevelopmentofsubsequentstatesofthenetworkandfacilitatesacoherentprogressionofcognitiveprocesseswithnoneedforaseparate,higher-orderexecutivesystem.ThelefthemisphereplaysauniqueroleinshapingthecontentsofsubjectiveexperienceStudiesofsplit-brainpatientsrevealthatthelefthemi-sphereofthehumanbrainhasauniquecapacitytoreexivelyformulatecausaltheoriesaboutwhyevents[2,10,11].Theadaptivebenetofsuchaprocessisimmense,enablinginformationfromdiverseeventstobecombinedintoachainofcausalunderstandingthatcanguidefuturebehavior.Althoughthemechanismthroughwhichtheinterpretiveprocessworksisnotwellunder-stood,itappearstobeaninherentpropertyoftheinteractionsofcomponentsofthesystem,anditsfunctioninshapingthecontentsofconsciousexperienceissignicant.Strikingly,studiesofbothsplit-brainandneurologicallynormalindividualsindicatethattheinter-pretiveprocesscontinuestofunctionwhentherangeofavailableinformationisincomplete.Thisgeneratesacausalunderstandingofeventsthatissubjectivelycompleteandseeminglyself-evident,evenwhenthatunderstandingisincorrect[10,11,19]Fig.1).Inthework-spacemodel,thisresultcouldarisefromtheintegrationofinformationfromanincompletesetofdata.Theprocesshasevolvedtoprovideacausalexplanationanddoesso,butwhentherangeofinformationavailabletotheworkspaceislimitedbecauseofdamagetotheneuralFig.1.Studiesofsplit-brainpatientsrevealthatthelefthemisphereautomaticallyconstructsasubjectiveunderstandingofinformationavailabletoit.(a)Inaclassicexampleofthisprocess,apictureofachickenclawwasbrießypresentedtothe(speaking)lefthemisphere,whileasnowscenewasconcurrentlyshowntothe(silent)righthemisphere.Aftertheseinitialimageswereremoved,patientPSeasilypickedoutrelatedpicturesfromasetofeightchoices,whichremainedonthescreen.Hislefthandpointedtoasnowshovelandhisrighthandpointedtoachicken,andbothhemisphereswereabletoobservethesechoices.Whenaskedwhyhehadpickedthoseparticu-larpictures,PSsaidÔOh,that’ssimple.Thechickenclawgoeswiththechicken,andyouneedashoveltocleanoutthechickenshed.Õ(ReproducedwithpermissionfromRef.[26].)(b)Presentationofacommandtothenon-speakingrighthemispheregeneratesbehaviorbaseduponinformationwhichisunavailabletothelefthemiAftertheactionisperformed,however,thespeakinglefthemisphereautomaticallygeneratesanunderstandingofthebehavior(twoexamplesgiven).Althoughtheunder-standingisincorrect,itisexperiencedbythathemisphereasanaccuratedescriptionoftheevent.(AdaptedwithpermissionfromRef.[26] TRENDS in Cognitive Sciences (b) TRENDSinCognitiveSciencesVol.7No.4April2003 processorsthatprovideinformationtothenetwork,theaccuracyoftheresultinginterpretationislimitedtotherestrictedrangeofavailableinformation.Interpretingapost-lesionworldWhenconsideredwithinaframeworkofmodular,inter-pretedconsciousness,avarietyofseeminglybizarreneurologicalsyndromesrevealarationalpatternofsymptoms.Althoughphenomenallydistinct,suchsyn-dromesmaybemechanisticallyrelated,withsymptomsfallingintoplaceasthelogicalresultsofaninterpretivesystemthatisstrivingtomakesenseofanalteredsetofavailableinformation.NeurologicallesionscanaffectperceptionandmemoryBecauseparticularlesionsleavepatientswithnoexperi-enceofdecit,itfollowsthatthesepatientsmusthaveasatisfactoryagreementbetweentheirpost-lesionexperi-enceandtheirpre-lesionmemories.Suchanextensionofneurologicalsymptomsintotherealmofmemoryhasbeendemonstratedinpatientswithhemispatialneglect,whoseleft-neglectedmemoriesmatchtheirleft-neglectedexperi-enceoftheworldworld.Inthemodular-consciousnessmodel,thisresultisnotsurprising.Becausetheneuralcorrelatesofconsciousnessareproposedtoconsistofactivityintheverynetworksthatareresponsibleforprocessingtherelevantinformationalattributes,thismodelpredictsthatfocallesionsmighthavedramaticeffectsonspecicaspectsofconsciousexperience,includ-ingtheirrepresentationinmemory.Justasparticularcapacities,suchasfacerecognition,generationofnounsinspeechandmanipulationofobjectsinspacemightbeeitherimpairedoreliminatedbycorticaldamage,sotoomighttheabilitytoprocessandrepresentspecicaspectsofconsciousexperiencebeeitherimpairedorabolishedbyneurologicalinjury.Studiesindicatingthatretrievalofamemoryentailsactivationofthesameperceptualcircuitsthatareactivateddirectlybytheeventbeingrecalledrecalledcompletethepicture.Forpatientswithvisualhemine-glect,neglectoftheleftvisualeldoccursintherealmofmemory,justasitdoesduringactualperceptionofascene,althoughinformationaboutthecompletespatialsceneremainsencodedinthebrainbrain(Fig.2).Thecompletedmemorycannotbereconstructedfromanyonementalvantagepointbecause,fromeachperspective,theaspectsofthememorythatpertaintoleftvisualspacecannotreceivesufcientattentionalamplicationtoenabletheirlarge-scalerepresentationandavailabilityintheneuronalworkspace,and,thus,inconsciousexperience.Changingone’sperspectiveinthevisualimageenablestheinfor-mationneglectedfromonevantagepointtobecomeavailablefromthesecond.Thisisbecausethechangeinegocentriccoordinatesenablesinformationaboutthepreviouslyneglectedspacetobeprocessedbyneuralcircuitsthatareresponsibleforhandlinginformationaboutotherpartsofvisualspacethatremainabletoreceivethenecessaryattentionalamplicationtobringthestoredinformationintoconsciousness.Thepatient’sleft-neglectedmemoriesthereforedirectlyparallelhisleft-neglectedperceptionofthesurroundingworldbecausebothresultfromdamagetothesameprocessofattentionallocationintheworkspacenetwork.Lookingaroundafamiliarscene,everythingseemsjustasitshould,becausethememoryofthesceneisitselfleft-neglected.Ifaparticularlandmarkisnotobserved,theneglectpatientmightrotateuntilitcomesintoviewview,justasaneurologicallynormalindividualmightrotatetondsomethinglocatedbehindhim.Ineachcase,theindividualdrawsuponhismemory’srepresentationofthesceneandusesthistonavigatethroughhisconceptionofspace.Thepatientexperiencesnoalterationinperceptionbecausememoryandperceptionremaininagreement,withnodiscrepancytoindicateaproblem.FocallesionscanabolishtheabilitytoprocessentirerealmsofconceptualinformationLossoftheabilitytoprocessinformationaboutspecicaspectsofconsciousexperiencemightalsoaccountfortheinabilityofsomepatientstolearnoftheirimpairmentthroughothercognitivemeans.Thisinabilitytousesemanticknowledgetoanalyzetheirconditionremainspuzzling.However,thendingthatsomepatientswithanosognosiaforhemiplegiaareunabletoidentifyparaly-sisinthemselvesaswellasinothersothersindicatesthattheymighthavelosttheabilitytoprocessinformationaccuratelyfromtheentiredomaininwhichtheirimpair-mentexists.Theirbrainsareimpairedintheirabilitytoinstateworkspacestatesthatrepresentleft-bodyinfor-mationaboutthemselvesandothers,andsosuchinformationremainsexcludedfromtheiravailablerangeofconsciousexperience.Indicativeofthisredenitionoftherangeofconsciousexperience,onepatientexplainedthat‘Iknewthewordwasasortofmedicaltermforwhateverwaswrongbutthewordbotheredmebecauseyouonlyneglectsomethingthatisactuallythere,don’tyou?Ifit’snotthere,howcanyouneglectit?it?.WithnoFig.2.Inanexperimentdesignedtoassesstheeffectsofhemispatialneglectonmemoryrepresentationsons,patientswithlefthemineglectwereaskedtovisual-izethemselvesinapiazzafamiliartothembeforetheonsetofneglect,andtodescribethescenefromtheoppositeendsofthepiazza.Thedescriptionsprovidedfromeachimaginedpositionneglectedfeaturesofthecontralesionalsideofthescene,indicatingthatalthoughtheentirememorywaspreserved,theaspectsofthememorythatcouldbebroughtintoconsciousawarenessvariedsystematicallywiththeimaginedperspectiveofthepatient.Therefore,ifthepatientwereactuallytovisitthepiazza,therewouldbenodifferenceinthecomparisonofhispre-lesionmemorieswithhispost-lesionperceptualexperience,becausehisneglectaffectsconsciousexperienceofboththememoryandtheperception.(ReproducedwithpermissionfromRef.[26] TRENDS in Cognitive Sciences TRENDSinCognitiveSciencesVol.7No.4April2003 memoriestoindicateadecit,andwithanimpairedabilitytoprocessinformationthatisrelatedtotheexperientialrealminwhichthedecitexists,itbeginstobemoreunderstandablethatsomepatientscanbeunawareoftheirimpairments.DenialsofdecitresultfrominterpretationsofincompleteinformationIntheproposedmodel,thedenialsofdecitobservedinvisualneglectandanosognosiaforhemiplegiacanalsobeunderstoodasthelogicalresultsofdamagetospecicsetsofneuralcircuits.Whereasparalysisduetoseveringofnervesthatconnecttheparietalcortextothebodywouldbenotedimmediately,damagetothe(right)parietalcortexitselfleavesnopartofthebraintomonitororrepresenttheexistenceoflimbsontheleftsideofthebody.Theregionresponsibleforsignalingaproblemhas,itself,beendamaged,leavingnosystemtoleacomplaint.Therefore,thepatientnolongerregisterstheexistenceofleftlimbsbuthasanintactinterpretivenetworkthatconcludesthateverythingmustbenebecausenoproblemhasbeenindicatedinternally.Furthermore,becausetheworkspacenetworkcontainsnohigher-ordersystem,theabsenceofinformationabouttheleftsideofone’sbodyisnomoreworrisomethanalackofvisualinformationfrombehindone’shead–noimpairmentisregisteredbecausenoinputisexpected.Therefore,whenunabletodoabimanualtask,thesystemgeneratesareasonablestory,suchas‘Ididn’twanttodothattask.task..Presentedwithaparalyzedlefthand,andaccompaniedbyneithersensoryinputnorregistrationofthelackthereof,thesystemdrawsasubjectivelyreasonableconclusion:‘That’snotmyhandhand.Suchattemptsatrationalizationmimictheaccountsputforthbythespeakinglefthemispheresofsplit-brainpatientsfollowingright-hemisphere-generatedbehavior,andaremerelyextensionsoftheinterpretiveprocessesthatallowustomakesenseoftheworldaroundusonaneverydaybasis.Last,thedelusionsofreduplicativeparamnesiaareprimeexamplesofaninterpretivesystematworkwithacorruptedsetofinformation.Patientswiththissyndromeappeartohaveabnormalneuralindicatorsoffamiliarityandbelievethatmultiplecopiesofplacesandpeopleexistexist.WhilebeingexaminedatNewYorkHospital,onepatientwasconvincedthatshewasinherownhomeinFreeport,Maine.Althoughintelligentandawarethatherdoctorsdisagreedwithherassessment,sheremainedadamantinherassertions.Whenpressedtoexplainwhy,ifshewereindeedinherhouseinFreeport,therewasabankofelevatorsoutsidethedoor,sherepliedcalmly‘Doctor,doyouknowhowmuchitcostmetohavethoseputin?[11]Suchpatientsarestrikinglyunappable,incorporatingincongruousinformationwithease.Thewomaninthisexample‘knew’thatshewasinherownhouse,justasweknowwhenweareinours,andtheinterpretiveprocessesoftheworkspacenetworkmakessuchinformationseemself-evident,evenwhenitiswrong.However,althoughtheabilityofindividualswithdelusionalsyndromestocreateasubjectivelyrationalstoryoutofseeminglyincoherentinformationisstartling,whatmightbemoststrikingistherealizationthatsuchsyndromesrevealtheoverwhelmingsignicanceofthisprocessinshapingourownexperienceoftheworld.Theexplanationsprovidedbyaninterpretivesystemareonlyasgoodastheinformationavailabletoit,andbizarreinformationyieldsbizarreresults.Patientswithdelusionalsyndromesmightknowthattheirassertionssoundstrangetoothers,buttheyalso‘know’thatthescenetheyperceiveiscomplete,thatthehandpresentedtothemisnottheirs,andthattheyaresittingintheirownhomes.Theinformationpresentedbythemodularcomponentsoftheworkspacenetworkareallthatthebrainhasavailabletoit,andyieldssubjectiveexperiencesthatarejustasself-evidentandunassailableastheexperienceengenderedbyanyothernetworkstate.Thepresenceofsuchaninterpretivemechanismisbenecialinanintactbrainandonanevolutionaryscalebecauseitgreatlyenhancestheabilityofanindividualtoadapttoawiderangeofnovelandunexpectedsituations.However,itresultsinavarietyofstrangebeliefswhentheinternalinformationofthebrainisitselfcorrupted.Datafromawiderangeoffunctional,physiologicalandclinicalstudiessupportamodelofconsciousnessinwhichsubjectiveawarenessemergesfromtheinteractionsofspecialized,modularcomponentsinadistributedneuralnetwork.Inaddition,theactivityofsuchcomponentsisunitedcognitivelybyaninterpretiveprocessthatoccursinthelefthemisphereofthehumanbrain.Thedynamic,self-modifyingnatureoftheinteractionsbetweenthesecomponentsisdrivensolelybytherangeofinformationavailabletothesystemandenablesthecoherentpro-gressionofcognitiveprocesseswithoutrequiringahigher-orderexecutivesystem.Furthermore,thespecializednatureofthecomponentneuralprocessorssuggestsapotentialexplanationforhowspeciclesionscanselec-tivelyalteroreliminatethecontentsofparticularaspectsofsubjectiveexperience,withnoresultingexperienceofdecitforthebrain-damagedindividual.Althoughtheproposedmodelremainsindevelopmentasaconceptualframework,webelievethat,fortheavailabledata,amodelbasedontheinterpretedinte-grationofspecializedneuralprocessorshasnotableexplanatorypower.Furtherstudyisneededtobettercharacterizethenatureofthesemodularprocessorsandthewaysinwhichtheyinteract.Webelievethatsuchworkwillprovidesignicantinsightintotheprocessesthatunderlietheconstructionofsubjectiveexperience.1Ramachandran,V.S.(1995)Anosognosiainparietallobesyndrome.Conscious.Cogn.4,22–512Gazzaniga,M.S.(1989)Organizationoft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