The neuronal basis for consciousness

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Theneuronalbasisforconsciousness

R.Llinas,U.Ribary,D.ContrerasandC.PedroarenaDepartmentofPhysiologyandNeuroscience,NewYorkUniversitySchoolofMedicine,550FirstAvenue,NewYork,NY10016,USA

Attemptingtounderstandhowthebrain,asawhole,mightbeorganizedseems,forthe¢rsttime,tobeaserioustopicofinquiry.Oneaspectofitsneuronalorganizationthatseemsparticularlycentraltoglobalfunctionistherichthalamocorticalinterconnectivity,andmostparticularlythereciprocalnatureofthethalamocorticalneuronalloopfunction.Moreover,theinteractionbetweenthespeci¢candnon-speci¢cthalamicloopssuggeststhatratherthanagateintothebrain,thethalamusrepresentsahubfromwhichanysiteinthecortexcancommunicatewithanyothersuchsiteorsites.Thegoalofthispaperistoexplorethebasicassumptionthatlarge-scale,temporalcoincidenceofspeci¢candnon-speci¢cthalamicactivitygeneratesthefunctionalstatesthatcharacterizehumancognition.Keywords:consciousness;thalamocortical;gammaoscillations;facilitation;coincidencedetection;voltagesensitivedye

1.INTRODUCTIONPerhapsoneofthemostinsightfuldiscussionsrelatingtothenatureofglobalbrainfunctiontookplaceinEnglandinthe¢rstdecadesofthiscenturybetweenCharlesS.Sherrington(1906)andT.GrahamBrown(1915).Theformerproposed,onthebasisofanimalphysiologicalexperimentation,thatthespinalcordoperated,funda-mentally,asasetofcomplexre£exes.Indeed,thisviewfollowedtheJamesianpostulateofre£ex(James1890),inwhichthenervoussystemisorganizedasasetofcomplexneuronalconnectivitypathwaystriggeredintoactionbytheoutsideworld.Onthisview,behaviourisfundamen-tallytheresultantofsensoryinput.ThisgeneralpostulatecontrastedwiththepointofviewespousedbyGrahamBrown(1914,1915)andmorerecentlybyNicholasBern-stein(1967),whoviewedspinalcordfunctionasmostlyorganizedasintrinsicallygeneratedneuronalactivity.Withthisviewsensoryinputsaremostlymodi¢ersofsuchintrinsicactivity.Brownworked,asdidSherrington,onthespinalcordbutmorespeci¢callyonlocomotion.Hewasthe¢rsttodemonstratethatlocomotionwasstillsupportedbythespinalcordafterbilateraldorsalrootdea¡erentation,resultinginthetotalremovalofsensoryinput(Brown1914).Onthatbasis,heproposedthatthecomplexmotoroutputrequiredforlocomotionisapropertyofthespontaneousactivityoftheneuronalcircuitsinthespinalcordandbrainstem.Interestingly,suchimportantobservationandconclusionhavebeenmostlyignoredbypresent-dayneuroscience,whichcontinuestoemphasizetheprimordialimportanceofsensoryinputinmotororganization.Likewise,incognitivephysiologytheprevailingviewtodayisthatconsciousnessismostlytheresultantofsensoryinputbroughtintothebrainbythedi¡erentsensorya¡erents,theactivityofwhichrepresentthefunctionalbasisforcognition.2.COGNITIONASANINTRINSICFUNCTIONALSTATEOFTHEBRAINWeproposehere,aswehavedoneonpastoccasions(Llinas1990),thatconsciousness,likelocomotion,mightbemoreacaseofintrinsicactivitythanofsensorydrive.Thus,ithasbeenproposedthatconsciousnessisanoneiric-likeinternalfunctionalstatemodulated,ratherthangenerated,bythesenses(Llinas&Pare1991).Wemayrememberhowinchildhoodthesoundofacurtain£utteringinthedarkcouldevokeratherworryingimagesthatwereimmediatelydispelledbyturningonthelights.Andso,theinternaleventsthatweknowasthinking,imaginingorrememberingare,forthemostpart,relatedtointrinsicactivity.Thisisofcourseverymuchinaccordancewiththefactthataverylargepercentageoftheconnectivityinthebrainisrecurrentandthatmuchofitsactivityisrelatedtosuchintrinsicconnectivitynotnecessarilyrelatedtotheimmediacyofsensoryinput.Perhapsthemostspectaculardi¡erenceconcerningglobalbrainstatesisthatbetweenwakefulnessanddreamlesssleep.Weallrecognizethatnogrossmorpholo-gicalchangesoccurinourbrainsduringsleep,thatcouldexplaintheenormousdisparitybetweenthetwostates.Indeed,thedi¡erencemustbefunctional.Weknowfullwellthatifwearetiredwecanfallasleepextraordinarilyquicklyandthatifweareasleepandastrongstimulusisgiventous(e.g.thehavocplayedbyanalarmclock)wecanawakenalsoextraordinarilyfast.Itissofast,indeed,thattheonlysubstratecapableofsupportingthespeedofthesetwoeventsmustbeelectricalinnaturegiventhelargenumberofelementsinvolved;electricalinthesenseoftheelectricalactivityofneuronsandthesynapticinputthatinitiateorterminatesuchactivity.Thequestionswouldthenbe:(i)whatisthefunda-mentaldi¡erencebetweenbeingawakeandbeingasleep?and(ii)whatdoesittellusaboutbrainfunction?Itseemstousthattheseareamongthemostimportant

Phil.Trans.R.Soc.Lond.B(1998)353,1841^18491841&1998TheRoyal

Societycluesaboutthenatureofconsciousness.The¢rstconclusiontobedrawnfromsuchinferenceisthatconsciousness(i.e.beingawakeandabletofeel,judgeandremember)isbutonefunctionalstateofourbrain.Otherstates,suchasbeingasleep,donotsupportconsciousnessoreventhefeelingofself-existence.Fromclassicalneurologyweknowthatdamagetothecerebralcortexinmammalscancauseavarietyofwell-de¢neddysfunctionalconditionsorsyndromes.Visualcortexdamageisaccompaniedbyblindnessthatcanbeofdi¡erenttypesdependingonthepreciselocationofthecorticalinsult.Similar¢ndingsarealsoencounteredinothercorticalstructures.Thus,damagetotheauditory,thesomatosensory,themotorandpre-motorcorticesareaccompaniedbywell-de¢nedconditions.Infact,the¢rstsuchneurologicallesiontobedescribedinthetermsusedabovewasthatwhichfollowsdamageofBroca'sarea,generatingdysarthria.Giventheabove,wetendtoequateconsciousnesswithcorticalfunctionmoreorlessexclusively,ignoringthefactthatthenervoussystemisdeeplycursiveandthatastrictlyhierarchicalorganization,ratherthanaglobalorder,ismostunlikely.Ontheassumptionthatconscious-nessisaglobalfunctionalstateofthebrainrelatingtomorethancorticalactivity,weshallnowattempttode¢nethefunctionalparametersthatsupportandgenerateconsciousness.